R E S E A R CH P A P E R

The roles of dispersal and mass extinction in shaping palmdiversity across the Caribbean

Angela Cano12 | Christine D Bacon23 | Fred W Stauffer1 |

Alexandre Antonelli234 | Martha L Serrano-Serrano5 | Mathieu Perret1

1Conservatoire et Jardin botaniques de la

Ville de Geneve and Department of Botany

and Plant Biology University of Geneva

Chambesy Geneva Switzerland

2Gothenburg Global Biodiversity Centre

Geurooteborg Sweden

3Department of Biological and

Environmental Sciences University of

Gothenburg Geurooteborg Sweden

4Gothenburg Botanical Garden Geurooteborg

Sweden

5Department of Ecology and Evolution

University of Lausanne Lausanne

Switzerland

CorrespondenceAngela Cano Conservatoire et Jardin

botaniques de la Ville de Geneve Chambesy

Geneva Switzerland

Email angelacano11gmailcom

Funding information

European Research Council GrantAward

Number 331024 Vetenskapsradet Grant

Award Number B0569601 Swiss National

Science Foundation GrantAward Number

31003A_1756551

Editor Lyn Cook

Abstract

Aim The rich flora of the Caribbean islands and surrounding mainland evolved in a

context of isolation alternated with phases of terrestrial connectivity between land-

masses climatic fluctuations and episodes of mass extinctions during the Cenozoic

We explored how these events affected the evolution of the sister palm tribes

Cryosophileae and Sabaleae and how continent-island exchanges endemic radia-

tions and mass extinction shaped their extant diversity

Location The American continent including the Caribbean region

Methods We reconstructed a time-calibrated phylogeny of the palm tribes Cryoso-

phileae and Sabaleae using 84 of the known species We inferred ancestral distri-

bution and tested the effect of island colonization and mass extinction on extant

diversity

Results Our results indicate that Cryosophileae and Sabaleae originated c 77 Ma

most probably in Laurasia and their extant species started to diversify between 56ndash

35 Ma and 19ndash10 Ma respectively Biogeographical state reconstruction estimated

that Cryosophileae dispersed to South America between 56ndash35 Ma then dispersed to

North-Central America between 39ndash25 Ma and the Caribbean islands between 34ndash

21 Ma We detected a possible signature of a mass extinction event at the end of the

Eocene affecting the diversification of Cryosophileae and Sabaleae and we did not

detect a diversification rate shift related to the colonization of the Caribbean islands

Main conclusions Species of Cryosophileae in the Caribbean islands are probably

derived from a single Oligocene dispersal event that likely occurred overwater from

North-Central America rather than through the hypothesized GAARlandia land

bridge Contrastingly three independent Miocene dispersal events from North-Cen-

tral America explain the occurrence of Sabaleae in the Caribbean islands Contrary

to our expectations island colonization did not trigger increased diversification

Instead we find that diversification patterns in this clade and its disappearance

from northernmost latitudes could be the signature of a mass extinction triggered

by the global temperature decline at the end of the Eocene

K E YWORD S

Arecaceae Boreotropical migrations Caribbean Coryphoideae diversification mass extinction

overwater dispersal palms Sabal West Indies

DOI 101111jbi13225

Journal of Biogeography 20181ndash12 wileyonlinelibrarycomjournaljbi copy 2018 John Wiley amp Sons Ltd | 1

1 | INTRODUCTION

The Americas have experienced dramatic geological changes over

the past 100 Myr North America was temporarily connected to Eur-

asia through the North Atlantic and Beringian land bridges (Brikiatis

2014 and references therein) Central America was hit by a massive

meteorite (Schulte et al 2010) the Caribbean islands emerged and

drifted eastwards in the Caribbean Sea (Iturralde-Vinent amp MacPhee

1999) and South America ended its isolation with the formation of

the Panama Isthmus (Montes et al 2015) How these events influ-

enced the outstanding biodiversity of the Neotropics has been a

subject of long-standing discussion (Antonelli amp Sanmartın 2011a)

renewed in recent years with the advent of new molecular dating

and biogeographical methods and cross-taxonomic comparative

analyses (eg Bacon et al 2015 Hoorn et al 2010 OrsquoDea et al

2016 Rull 2011) In this context the Andean and Amazonian

regions have drawn the most attention while much less effort has

been devoted to understanding the evolution of the Caribbean in

particular its flora

The sister palm tribes Cryosophileae and Sabaleae (subfamily

Coryphoideae) known as the New World Thatch Palms (NWTP

Dransfield et al 2008) have evolved in the dynamic context of the

Caribbean They are currently restricted to the Caribbean islands (34

species most of them in the Greater Antilles) and nearby landmasses

of North-Central America (25 species) and South America (10 spe-

cies) (Henderson Galeano amp Bernal 1995) However they had a lar-

ger past distribution in the Northern hemisphere as evidenced by

their extensive fossil record (Figure 1) that dates to the Late Creta-

ceous (Manchester Lehman amp Wheeler 2010) Combining these

fossil data with a phylogeny of extant NWTP species would help

retrace their evolution in time and space and illuminate the origin

and diversification of the Caribbean flora

The Caribbean region including the Greater and Lesser Antilles

contains about 13000 seed plant species Of these 72 are ende-

mic to the region and at least 10 are either endangered or critically

endangered sensu the International Union for Conservation of Nat-

ure (Acevedo-Rodrıguez amp Strong 2008 Oleas et al 2013) Com-

parative studies have shown a floristic affinity between the

Caribbean islands and the surrounding mainland (Acevedo-Rodrıguez

amp Strong 2008) but our understanding of the underlying evolution-

ary processes that shaped this diversity is still limited (Francisco-

Ortega et al 2007 Graham 2003 Nieto-Blazquez Antonelli amp

Roncal 2017 Santiago-Valentin amp Olmstead 2004) Available bio-

geographical studies focused on Caribbean plants point to multiple

biotic exchanges among the islands between North-Central America

and South America and local diversifications (Cervantes Fuentes

Gutierrez Magallon amp Borsch 2016 van Ee Berry Riina amp

Gutierrez Amaro 2008 Santiago-Valentin amp Olmstead 2004) For

example the Caribbean Acalyphoideae (Euphorbiaceae) are esti-

mated to have repeatedly colonized the Caribbean islands during the

Miocene mainly from Central America (Cervantes et al 2016)

whereas Brunfelsia (Solanaceae) probably entered the Antilles 8ndash

6 Ma from South America (Filipowicz amp Renner 2012) Phylogenetic

studies in different palm lineages also indicate independent coloniza-

tions of the Caribbean islands from the mainland and multiple migra-

tions between North and South America (Bacon Baker amp Simmons

2012 Bacon Mora Wagner amp Jaramillo 2013 Cuenca Asmussen-

Lange amp Borchsenius 2008 Roncal Zona amp Lewis 2008) For the

NWTP previous phylogenetic hypotheses have suggested an origin

of the Caribbean taxa from a mainland ancestor (Roncal et al 2008)

However a better resolved phylogeny is needed to trace whether

their diversity in the Caribbean is the result of multiple mainland-

island dispersal events or a colonization event followed by local

diversification

Several geological models have been hypothesized to facilitate

interchanges between land areas around the Caribbean region These

include the Proto-Antilles connecting North to South America during

the Late Cretaceous to the Palaeocene (94ndash63 Ma Graham 2003)

the Greater Antilles-Aves Ridge (GAARlandia) connecting the West

Indies to South America during the Oligocene (35ndash33 Ma Iturralde-

F IGURE 1 Distribution of extant Cryosophileae and Sabaleae (pink area) and fossils related to them from different epochs Late Cretaceous(black 100ndash66 Ma) Paleogene (grey 66ndash23 Ma) Neogene (white 23ndash26 Ma) Shapes represent different taxonomic groups triangleCryosophileae square Sabal circle Sabalites See Appendix S1 for data sources Map projection sphere Mollweide (53009)

2 | CANO ET AL

Vinent amp MacPhee 1999) and the Panama Isthmus formation start-

ing in the Miocene (Montes et al 2015) To what extent these puta-

tive corridors facilitated species dispersal across the Caribbean

region is still debated (eg Ali 2012 Nieto-Blazquez et al 2017)

and several studies postulate that overwater dispersal events have

played a major role in the biogeographical history of Caribbean plant

lineages (Cervantes et al 2016 Gugger amp Cavender-Bares 2013)

In addition to dispersal the dynamics of speciation and extinc-

tion during the history of lineages may also have influenced the cur-

rent patterns of species richness across the Caribbean and

surrounding areas (Ricklefs amp Bermingham 2008) The colonization

of archipelagos has been frequently associated with an increase of

morphological and taxonomic diversity (Bacon et al 2012 Baldwin

amp Sanderson 1998 Condamine Leslie amp Antonelli 2016 Losos amp

Ricklefs 2009) The diversification rate shift estimated for the Carib-

bean Coccothrinax (Baker amp Couvreur 2013b) the most diverse

genus of the NWTP is congruent with the hypothesis of a species

radiation triggered by island colonization Alternatively mass extinc-

tion events could also have influenced how diversity accumulated

through time (Antonelli amp Sanmartın 2011b Brocklehurst Ruta

Meurouller amp Freuroobisch 2015 Crisp amp Cook 2009) In particular three

episodes of relatively rapid climatic cooling could have affected the

diversity of frost-intolerant plants in the Caribbean region (1) the

CretaceousndashPalaeogene Event (66 Ma) when a large meteorite

impacted the Yucatan Peninsula generating immediate global dark-

ness and cooling (Schulte et al 2010) (2) the Terminal Eocene

Event (35 Ma) when global temperatures drastically dropped nega-

tively affecting the Boreotropical flora that covered large parts of

Laurasia (Morley 2003) and (3) the period following the mid-Mio-

cene climatic optimum (12 Ma) when globally warm equable cli-

mates shifted to present-day cooler and more seasonal climates

(Zachos Dickens amp Zeebe 2008) It remains unclear if the NWTP

which are considered typical elements of the Boreotropical flora

(Bjorholm Svenning Baker Skov amp Balslev 2006) were more

affected by Cenozoic cooling that caused their extirpation from Eur-

asia and northern North America (Figure 1) or by the meteorite

impact in the vicinity of their distribution range

We generated a time-calibrated species phylogeny of the NWTP

and used it to infer the biogeographical scenario that best explains

their current distribution and diversity We addressed the following

specific questions (1) When and where did the NWTP originate (2)

Is their diversity in the Caribbean the result of one or multiple dis-

persal events and which colonization routes did they follow (3)

How did island colonization and global episodes of mass extinction

influence extant NWTP diversity across the Caribbean and surround-

ing areas

2 | MATERIALS AND METHODS

21 | Taxon sampling

Our sampling includes 89 accessions from 67 species Sampling in

Cryosophileae (11 genera 35 species of 42) is complete except in

the genera Cryosophila (7 species of 10 sensu Evans 1995) and Coc-

cothrinax (10 species of 14 sensu Henderson et al 1995) Sampling

in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe-

cies of Sabal (Dransfield et al 2008) To evaluate the phylogenetic

position of the NWTP within Coryphoideae we also sampled repre-

sentatives of other tribes in this subfamily Two outgroups were

selected in subfamilies Ceroxyloideae and Arecoideae Silica-gel dried

leaf fragments were collected in the field (collection and export per-

mits 111296 and 113458 respectively from the Paraguayan Secre-

tarıa del Ambiente) or in the living collections of the Conservatoire et

Jardin botaniques de la Ville de Geneve (Switzerland) Montgomery

Botanical Center Fairchild Tropical Botanical Garden (both in the

USA) and the Jardın Botanico del Quindıo (Colombia) Voucher infor-

mation is provided in Table S11 (see Appendix S1 in Supporting

Information)

22 | Phylogenetic analyses

Four nuclear (CISP4 CISP5 PRK and RPB2) and one plastid (matK)

loci were sequenced following the protocol described in

Appendix S1 and using the primers listed in Table S12 The DNA

sequences are deposited in GenBank under the accession numbers

listed in Table S11 Sequences were aligned using MAFFT 7130

(Katoh Misawa Kuma amp Miyata 2002) Sites were scored with

GUIDANCE 141 (Penn et al 2010) and excluded from further analy-

ses if their score was lt08 to avoid adding noise to the branch

length and substitution rate estimates (Jordan amp Goldman 2012)

The final database contained 4872 bp Phylogenetic analyses were

performed on the CIPRES portal (Miller Pfeiffer amp Schwartz 2010)

Single-gene and combined partitioned phylogenetic analyses were

carried out with MRBAYES 322 (Ronquist et al 2012) In the parti-

tioned analyses the dataset was divided into five partitions corre-

sponding to each marker The best fitting substitution model for

each partition was selected from 24 models with MRAICPL 146

(Nylander 2004) using the Akaike information criterion (AIC) The

test selected the models HKY for CISP4 CISP5 and PRK GTR for

matK and GTR+Γ for RPB2 Four Markov chains were run for

5 9 106 generations with a heating temperature of 015 Samples

were logged every 100th generation Using TRACER 16 (Rambaut

Suchard Xie amp Drummond 2014) we determined burnin (24) and

confirmed trace stationarity and sufficient sampling (effective sample

size [ESS] gt200)

23 | Fossil calibration and divergence time analyses

Three fossils were used to estimate divergence times (Table S13)

Following Couvreur Forest and Baker (2011) fossils of Sabalites

carolinensis Berry and Hyphaene kappelmanii Pan et al were used to

constrain the stem nodes of subfamily Coryphoideae and subtribe

Hyphaeninae (Coryphoideae) respectively In addition fossilized

seeds of Sabal bigbendense (Manchester et al 2010) were used to

calibrate the stem node of Sabaleae These seeds from the Late Cre-

taceous (c 77 Ma) represent the oldest record attributed to the

CANO ET AL | 3

tribe Since the use of this fossil for calibrating the NWTPrsquos phy-

logeny has a strong effect on the divergence time estimates (Fig-

ure S11) a close evaluation of its relationship with the extant genus

Sabal was conducted and its classification within Sabaleae was sup-

ported (Appendix S1)

Divergence time analyses were conducted in BEAST 180 (Drum-

mond Suchard Xie amp Rambaut 2012) applying the same partitions

and substitution models as for MRBAYES Substitution and clock mod-

els were set as unlinked whereas tree models were linked among

partitions Clock model tests using stepping-stone sampling (SSS)

and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured

a relaxed clock with an uncorrelated lognormal distribution (UCLN

marginal log-likelihood = 2364194 BF = 111167) against a strict

clock (marginal log-likelihood = 2419777) We used uniform distri-

butions for UCLN mean priors for each data partition with default

initial and lower values and upper values set to 100 To assess the

impact of tree-model selection on our divergence time estimations

we compared the median node ages obtained with a Yule versus a

BirthndashDeath process model The differences ranged from 010 to

225 Ma and were markedly smaller than the 95 HPD age bars for

each model (Figure S12) indicating that both tree models yield simi-

lar divergence time estimations Because tree-model tests strongly

favoured a Yule Process (marginal log-likelihood = 2364194

BF = 7165) over a BirthndashDeath process (marginal log-

likelihood = 2367776) the Yule tree model was implemented in

further analyses

To account for uncertainty in fossil dating and identification

soft-bound lognormal priors were used for all calibration points with

standard deviations set such that 95 of the age distribution fell

within the geological time period of the fossil stratigraphic source

(Table S13 Yang amp Rannala 2006) Seven independent chains were

run for 50 9 106 generations sampling every 10000th generation

All the chains converged and their ESS values were above 200

Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-

TOR 180 (Drummond et al 2012) was used to exclude the adequate

proportion of burnin samples and obtain a maximum clade credibility

(MCC) tree displaying median heights

24 | Biogeographical analyses

Five biogeographical areas were defined (O) Old World (N) North-

Central America (S) South America (I) Panama Isthmus delimited

between the El Valle area (Panama) and the Uramita suture

(Colombia Montes et al 2015) and (C) Caribbean islands The lat-

ter were treated as a single area to facilitate understanding of bio-

tic exchanges amongst insular-continental regions A distinction

between the Greater and the Lesser Antilles was not appropriate

since most of the NWTP species occur in the Greater Antilles (34

species) and only two widespread species are present in the Lesser

Antilles Species distributions were compiled from the literature

(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans

1995 Henderson et al 1995 Zona 1990) and from the Global

Biodiversity Information Facility (GBIF httpwwwgbiforg

accessed 17 July 2014) Conflicting occurrences from GBIF (eg

palms cultivated in botanic gardens) were excluded

We inferred the biogeographical history of the NWTP using the

Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)

model (Ree amp Smith 2008) with and without the parameter ldquojrdquo

accounting for the probability of founder-event speciation as imple-

mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The

DEC+j model is appropriate in this study since the NWTP occur in

areas that have been isolated (South America the Caribbean islands)

and therefore instantaneous speciation in conjunction with long-dis-

tance dispersal may be expected Analyses were applied to the MCC

tree and tree uncertainty was considered for the interpretation of

results The tree was pruned to include a single terminal per species

The maximum number of areas at nodes was restricted to three to

simplify the computational effort and because three is the maximum

number of areas currently inhabited by any NWTP species Analyses

were conducted with and without dispersal constraints Dispersal

constraints (Table S14) were applied by assigning different dispersal

probabilities as follows p = 1 for dispersal between adjacent areas

p = 5 for dispersal over the Caribbean Sea or through non-adjacent

land areas (eg between N and S) and p = 01 for dispersal over the

Atlantic Ocean (eg between S and O) or across the fully formed

Northern Andes barrier As a sensitivity test to parameter choice

when the lowest dispersal probability was set to 01 instead of 001

no significant differences were found in the biogeographical recon-

struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141

lnL difference lt2 log-likelihood units) and relative probabilities (Fig-

ure S13)

Four time periods were defined (1) 90ndash33 Ma probability of dis-

persal from areas O to N through the Beringian and North Atlantic

land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the

Northern Hemisphere were no longer available (Brikiatis 2014) (3)

15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)

7 Ma-present final uplift of the Northern Andes acting as a barrier

for dispersal between Amazonia and Choco (Luebert amp Weiged

2014 Table S15)

25 | Diversification analyses

We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the

existence (if any) and number of diversification rate shifts in the

NWTP phylogeny A set of 120 trees were randomly chosen from

the BEAST sampling to calculate maximum likelihood estimates of spe-

ciation and extinction rates and rate shift times The function

bdshiftsoptimum was set to optimize the model parameters in 100

iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma

(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect

[Nee Holmes May amp Harvey 1994]) To determine how many rate

shifts are most probable given the phylogenies models with n and

n + 1 shifts were compared with likelihood ratio tests following the

greedy approach by Stadler (2011a) Mean and standard deviation of

diversification rates and shift ages were calculated across the 120

trees

4 | CANO ET AL

Vinent amp MacPhee 1999) and the Panama Isthmus formation start-

ing in the Miocene (Montes et al 2015) To what extent these puta-

tive corridors facilitated species dispersal across the Caribbean

region is still debated (eg Ali 2012 Nieto-Blazquez et al 2017)

and several studies postulate that overwater dispersal events have

played a major role in the biogeographical history of Caribbean plant

lineages (Cervantes et al 2016 Gugger amp Cavender-Bares 2013)

In addition to dispersal the dynamics of speciation and extinc-

tion during the history of lineages may also have influenced the cur-

rent patterns of species richness across the Caribbean and

surrounding areas (Ricklefs amp Bermingham 2008) The colonization

of archipelagos has been frequently associated with an increase of

morphological and taxonomic diversity (Bacon et al 2012 Baldwin

amp Sanderson 1998 Condamine Leslie amp Antonelli 2016 Losos amp

Ricklefs 2009) The diversification rate shift estimated for the Carib-

bean Coccothrinax (Baker amp Couvreur 2013b) the most diverse

genus of the NWTP is congruent with the hypothesis of a species

radiation triggered by island colonization Alternatively mass extinc-

tion events could also have influenced how diversity accumulated

through time (Antonelli amp Sanmartın 2011b Brocklehurst Ruta

Meurouller amp Freuroobisch 2015 Crisp amp Cook 2009) In particular three

episodes of relatively rapid climatic cooling could have affected the

diversity of frost-intolerant plants in the Caribbean region (1) the

CretaceousndashPalaeogene Event (66 Ma) when a large meteorite

impacted the Yucatan Peninsula generating immediate global dark-

ness and cooling (Schulte et al 2010) (2) the Terminal Eocene

Event (35 Ma) when global temperatures drastically dropped nega-

tively affecting the Boreotropical flora that covered large parts of

Laurasia (Morley 2003) and (3) the period following the mid-Mio-

cene climatic optimum (12 Ma) when globally warm equable cli-

mates shifted to present-day cooler and more seasonal climates

(Zachos Dickens amp Zeebe 2008) It remains unclear if the NWTP

which are considered typical elements of the Boreotropical flora

(Bjorholm Svenning Baker Skov amp Balslev 2006) were more

affected by Cenozoic cooling that caused their extirpation from Eur-

asia and northern North America (Figure 1) or by the meteorite

impact in the vicinity of their distribution range

We generated a time-calibrated species phylogeny of the NWTP

and used it to infer the biogeographical scenario that best explains

their current distribution and diversity We addressed the following

specific questions (1) When and where did the NWTP originate (2)

Is their diversity in the Caribbean the result of one or multiple dis-

persal events and which colonization routes did they follow (3)

How did island colonization and global episodes of mass extinction

influence extant NWTP diversity across the Caribbean and surround-

ing areas

2 | MATERIALS AND METHODS

21 | Taxon sampling

Our sampling includes 89 accessions from 67 species Sampling in

Cryosophileae (11 genera 35 species of 42) is complete except in

the genera Cryosophila (7 species of 10 sensu Evans 1995) and Coc-

cothrinax (10 species of 14 sensu Henderson et al 1995) Sampling

in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe-

cies of Sabal (Dransfield et al 2008) To evaluate the phylogenetic

position of the NWTP within Coryphoideae we also sampled repre-

sentatives of other tribes in this subfamily Two outgroups were

selected in subfamilies Ceroxyloideae and Arecoideae Silica-gel dried

leaf fragments were collected in the field (collection and export per-

mits 111296 and 113458 respectively from the Paraguayan Secre-

tarıa del Ambiente) or in the living collections of the Conservatoire et

Jardin botaniques de la Ville de Geneve (Switzerland) Montgomery

Botanical Center Fairchild Tropical Botanical Garden (both in the

USA) and the Jardın Botanico del Quindıo (Colombia) Voucher infor-

mation is provided in Table S11 (see Appendix S1 in Supporting

Information)

22 | Phylogenetic analyses

Four nuclear (CISP4 CISP5 PRK and RPB2) and one plastid (matK)

loci were sequenced following the protocol described in

Appendix S1 and using the primers listed in Table S12 The DNA

sequences are deposited in GenBank under the accession numbers

listed in Table S11 Sequences were aligned using MAFFT 7130

(Katoh Misawa Kuma amp Miyata 2002) Sites were scored with

GUIDANCE 141 (Penn et al 2010) and excluded from further analy-

ses if their score was lt08 to avoid adding noise to the branch

length and substitution rate estimates (Jordan amp Goldman 2012)

The final database contained 4872 bp Phylogenetic analyses were

performed on the CIPRES portal (Miller Pfeiffer amp Schwartz 2010)

Single-gene and combined partitioned phylogenetic analyses were

carried out with MRBAYES 322 (Ronquist et al 2012) In the parti-

tioned analyses the dataset was divided into five partitions corre-

sponding to each marker The best fitting substitution model for

each partition was selected from 24 models with MRAICPL 146

(Nylander 2004) using the Akaike information criterion (AIC) The

test selected the models HKY for CISP4 CISP5 and PRK GTR for

matK and GTR+Γ for RPB2 Four Markov chains were run for

5 9 106 generations with a heating temperature of 015 Samples

were logged every 100th generation Using TRACER 16 (Rambaut

Suchard Xie amp Drummond 2014) we determined burnin (24) and

confirmed trace stationarity and sufficient sampling (effective sample

size [ESS] gt200)

23 | Fossil calibration and divergence time analyses

Three fossils were used to estimate divergence times (Table S13)

Following Couvreur Forest and Baker (2011) fossils of Sabalites

carolinensis Berry and Hyphaene kappelmanii Pan et al were used to

constrain the stem nodes of subfamily Coryphoideae and subtribe

Hyphaeninae (Coryphoideae) respectively In addition fossilized

seeds of Sabal bigbendense (Manchester et al 2010) were used to

calibrate the stem node of Sabaleae These seeds from the Late Cre-

taceous (c 77 Ma) represent the oldest record attributed to the

CANO ET AL | 3

tribe Since the use of this fossil for calibrating the NWTPrsquos phy-

logeny has a strong effect on the divergence time estimates (Fig-

ure S11) a close evaluation of its relationship with the extant genus

Sabal was conducted and its classification within Sabaleae was sup-

ported (Appendix S1)

Divergence time analyses were conducted in BEAST 180 (Drum-

mond Suchard Xie amp Rambaut 2012) applying the same partitions

and substitution models as for MRBAYES Substitution and clock mod-

els were set as unlinked whereas tree models were linked among

partitions Clock model tests using stepping-stone sampling (SSS)

and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured

a relaxed clock with an uncorrelated lognormal distribution (UCLN

marginal log-likelihood = 2364194 BF = 111167) against a strict

clock (marginal log-likelihood = 2419777) We used uniform distri-

butions for UCLN mean priors for each data partition with default

initial and lower values and upper values set to 100 To assess the

impact of tree-model selection on our divergence time estimations

we compared the median node ages obtained with a Yule versus a

BirthndashDeath process model The differences ranged from 010 to

225 Ma and were markedly smaller than the 95 HPD age bars for

each model (Figure S12) indicating that both tree models yield simi-

lar divergence time estimations Because tree-model tests strongly

favoured a Yule Process (marginal log-likelihood = 2364194

BF = 7165) over a BirthndashDeath process (marginal log-

likelihood = 2367776) the Yule tree model was implemented in

further analyses

To account for uncertainty in fossil dating and identification

soft-bound lognormal priors were used for all calibration points with

standard deviations set such that 95 of the age distribution fell

within the geological time period of the fossil stratigraphic source

(Table S13 Yang amp Rannala 2006) Seven independent chains were

run for 50 9 106 generations sampling every 10000th generation

All the chains converged and their ESS values were above 200

Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-

TOR 180 (Drummond et al 2012) was used to exclude the adequate

proportion of burnin samples and obtain a maximum clade credibility

(MCC) tree displaying median heights

24 | Biogeographical analyses

Five biogeographical areas were defined (O) Old World (N) North-

Central America (S) South America (I) Panama Isthmus delimited

between the El Valle area (Panama) and the Uramita suture

(Colombia Montes et al 2015) and (C) Caribbean islands The lat-

ter were treated as a single area to facilitate understanding of bio-

tic exchanges amongst insular-continental regions A distinction

between the Greater and the Lesser Antilles was not appropriate

since most of the NWTP species occur in the Greater Antilles (34

species) and only two widespread species are present in the Lesser

Antilles Species distributions were compiled from the literature

(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans

1995 Henderson et al 1995 Zona 1990) and from the Global

Biodiversity Information Facility (GBIF httpwwwgbiforg

accessed 17 July 2014) Conflicting occurrences from GBIF (eg

palms cultivated in botanic gardens) were excluded

We inferred the biogeographical history of the NWTP using the

Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)

model (Ree amp Smith 2008) with and without the parameter ldquojrdquo

accounting for the probability of founder-event speciation as imple-

mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The

DEC+j model is appropriate in this study since the NWTP occur in

areas that have been isolated (South America the Caribbean islands)

and therefore instantaneous speciation in conjunction with long-dis-

tance dispersal may be expected Analyses were applied to the MCC

tree and tree uncertainty was considered for the interpretation of

results The tree was pruned to include a single terminal per species

The maximum number of areas at nodes was restricted to three to

simplify the computational effort and because three is the maximum

number of areas currently inhabited by any NWTP species Analyses

were conducted with and without dispersal constraints Dispersal

constraints (Table S14) were applied by assigning different dispersal

probabilities as follows p = 1 for dispersal between adjacent areas

p = 5 for dispersal over the Caribbean Sea or through non-adjacent

land areas (eg between N and S) and p = 01 for dispersal over the

Atlantic Ocean (eg between S and O) or across the fully formed

Northern Andes barrier As a sensitivity test to parameter choice

when the lowest dispersal probability was set to 01 instead of 001

no significant differences were found in the biogeographical recon-

struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141

lnL difference lt2 log-likelihood units) and relative probabilities (Fig-

ure S13)

Four time periods were defined (1) 90ndash33 Ma probability of dis-

persal from areas O to N through the Beringian and North Atlantic

land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the

Northern Hemisphere were no longer available (Brikiatis 2014) (3)

15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)

7 Ma-present final uplift of the Northern Andes acting as a barrier

for dispersal between Amazonia and Choco (Luebert amp Weiged

2014 Table S15)

25 | Diversification analyses

We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the

existence (if any) and number of diversification rate shifts in the

NWTP phylogeny A set of 120 trees were randomly chosen from

the BEAST sampling to calculate maximum likelihood estimates of spe-

ciation and extinction rates and rate shift times The function

bdshiftsoptimum was set to optimize the model parameters in 100

iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma

(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect

[Nee Holmes May amp Harvey 1994]) To determine how many rate

shifts are most probable given the phylogenies models with n and

n + 1 shifts were compared with likelihood ratio tests following the

greedy approach by Stadler (2011a) Mean and standard deviation of

diversification rates and shift ages were calculated across the 120

trees

4 | CANO ET AL

tribe Since the use of this fossil for calibrating the NWTPrsquos phy-

logeny has a strong effect on the divergence time estimates (Fig-

ure S11) a close evaluation of its relationship with the extant genus

Sabal was conducted and its classification within Sabaleae was sup-

ported (Appendix S1)

Divergence time analyses were conducted in BEAST 180 (Drum-

mond Suchard Xie amp Rambaut 2012) applying the same partitions

and substitution models as for MRBAYES Substitution and clock mod-

els were set as unlinked whereas tree models were linked among

partitions Clock model tests using stepping-stone sampling (SSS)

and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured

a relaxed clock with an uncorrelated lognormal distribution (UCLN

marginal log-likelihood = 2364194 BF = 111167) against a strict

clock (marginal log-likelihood = 2419777) We used uniform distri-

butions for UCLN mean priors for each data partition with default

initial and lower values and upper values set to 100 To assess the

impact of tree-model selection on our divergence time estimations

we compared the median node ages obtained with a Yule versus a

BirthndashDeath process model The differences ranged from 010 to

225 Ma and were markedly smaller than the 95 HPD age bars for

each model (Figure S12) indicating that both tree models yield simi-

lar divergence time estimations Because tree-model tests strongly

favoured a Yule Process (marginal log-likelihood = 2364194

BF = 7165) over a BirthndashDeath process (marginal log-

likelihood = 2367776) the Yule tree model was implemented in

further analyses

To account for uncertainty in fossil dating and identification

soft-bound lognormal priors were used for all calibration points with

standard deviations set such that 95 of the age distribution fell

within the geological time period of the fossil stratigraphic source

(Table S13 Yang amp Rannala 2006) Seven independent chains were

run for 50 9 106 generations sampling every 10000th generation

All the chains converged and their ESS values were above 200

Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-

TOR 180 (Drummond et al 2012) was used to exclude the adequate

proportion of burnin samples and obtain a maximum clade credibility

(MCC) tree displaying median heights

24 | Biogeographical analyses

Five biogeographical areas were defined (O) Old World (N) North-

Central America (S) South America (I) Panama Isthmus delimited

between the El Valle area (Panama) and the Uramita suture

(Colombia Montes et al 2015) and (C) Caribbean islands The lat-

ter were treated as a single area to facilitate understanding of bio-

tic exchanges amongst insular-continental regions A distinction

between the Greater and the Lesser Antilles was not appropriate

since most of the NWTP species occur in the Greater Antilles (34

species) and only two widespread species are present in the Lesser

Antilles Species distributions were compiled from the literature

(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans

1995 Henderson et al 1995 Zona 1990) and from the Global

Biodiversity Information Facility (GBIF httpwwwgbiforg

accessed 17 July 2014) Conflicting occurrences from GBIF (eg

palms cultivated in botanic gardens) were excluded

We inferred the biogeographical history of the NWTP using the

Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)

model (Ree amp Smith 2008) with and without the parameter ldquojrdquo

accounting for the probability of founder-event speciation as imple-

mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The

DEC+j model is appropriate in this study since the NWTP occur in

areas that have been isolated (South America the Caribbean islands)

and therefore instantaneous speciation in conjunction with long-dis-

tance dispersal may be expected Analyses were applied to the MCC

tree and tree uncertainty was considered for the interpretation of

results The tree was pruned to include a single terminal per species

The maximum number of areas at nodes was restricted to three to

simplify the computational effort and because three is the maximum

number of areas currently inhabited by any NWTP species Analyses

were conducted with and without dispersal constraints Dispersal

constraints (Table S14) were applied by assigning different dispersal

probabilities as follows p = 1 for dispersal between adjacent areas

p = 5 for dispersal over the Caribbean Sea or through non-adjacent

land areas (eg between N and S) and p = 01 for dispersal over the

Atlantic Ocean (eg between S and O) or across the fully formed

Northern Andes barrier As a sensitivity test to parameter choice

when the lowest dispersal probability was set to 01 instead of 001

no significant differences were found in the biogeographical recon-

struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141

lnL difference lt2 log-likelihood units) and relative probabilities (Fig-

ure S13)

Four time periods were defined (1) 90ndash33 Ma probability of dis-

persal from areas O to N through the Beringian and North Atlantic

land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the

Northern Hemisphere were no longer available (Brikiatis 2014) (3)

15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)

7 Ma-present final uplift of the Northern Andes acting as a barrier

for dispersal between Amazonia and Choco (Luebert amp Weiged

2014 Table S15)

25 | Diversification analyses

We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the

existence (if any) and number of diversification rate shifts in the

NWTP phylogeny A set of 120 trees were randomly chosen from

the BEAST sampling to calculate maximum likelihood estimates of spe-

ciation and extinction rates and rate shift times The function

bdshiftsoptimum was set to optimize the model parameters in 100

iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma

(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect

[Nee Holmes May amp Harvey 1994]) To determine how many rate

shifts are most probable given the phylogenies models with n and

n + 1 shifts were compared with likelihood ratio tests following the

greedy approach by Stadler (2011a) Mean and standard deviation of

diversification rates and shift ages were calculated across the 120

trees

4 | CANO ET AL

To evaluate whether shifts in diversification rate could be attrib-

uted to a specific clade we used BAMM 20 (Rabosky 2014

Appendix S2) Controversy exists regarding the adequacy of BAMM

for diversification rate inference (Moore Hohna May Rannala amp

Huelsenbeck 2016) However recent evaluations of the method

suggested that diversification rate inference with BAMM is accurate

and consistent (Rabosky Mitchell amp Chang 2017) We used the

extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-

age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether

the colonization of the Caribbean islands was associated with shifts

in diversification rates (Appendix S2)

Finally to explore whether the temporal gap between stem and

crown ages observed in the NWTP phylogeny could be the signature

of mass extinction instead of low diversification followed by recent

radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-

dler 2011b) Following the approach by Antonelli and Sanmartın

(2011b) the shapes and the ages of Lineage Through Time (LTT)

curves of simulated trees were compared to the LTT curve observed

for the crown NWTP MCC tree Three sets of simulations were run

with the function simrateshifttaxa where only 5 of the lineages

survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-

minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)

In all sets the speciation (0223) and extinction (0180) rates were

kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200

trees were simulated to reflect stochastic variance with a final num-

ber of 54 terminals (the number of terminals in the crown NWTP

MCC tree) and accounting for the missing taxa with frac = 093

3 | RESULTS

31 | Phylogenetic analyses

The analyses of four independent loci support the sister relationship

between the tribes Cryosophileae and Sabaleae (posterior probability

[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister

in the CISP4 gene tree (Figure S21) but the alternative relationships

are not supported (PP lt 090) The comparison of individual gene

trees did not reveal other topological incongruences with PP gt095

MRBAYES and BEAST analyses of the combined partitioned dataset

recovered congruent results and the MCC tree from BEAST is shown

in Figure 2

32 | Divergence time and ancestral rangeestimation

Calibration analyses (Figure 2) inferred crown ages for the NWTP in

the Late Cretaceous (77 Ma [age values correspond to median

heights estimated with BEAST] 787ndash761 Ma [age ranges correspond

to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the

Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene

(14 Ma 187ndash96 Ma)

The most likely biogeographical model was DEC+j with dispersal

constraints (lnL = 914 Figure 3a) followed with a difference of

42 log-likelihood units by DEC with dispersal constraints

(lnL = 956) and by DEC+j without dispersal constraints

(lnL = 1024) Biogeographical analyses indicate that the NWTP

most probably originated in North America (pC = 045) sometime

during the Late Cretaceous By the Eocene Cryosophileae dispersed

to South America (pS = 067) giving rise to the genera Chelyocarpus

Itaya Sabinaria and Trithrinax Later during the early Oligocene

members of Cryosophileae dispersed back to North-Central America

and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)

Sabaleae most probably started diversifying in an area encompassing

both North America and the Caribbean islands (pNC = 050) or only

in North America (pN = 046) Two unambiguous dispersal events

from the continent to the Caribbean islands were inferred between

15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)

33 | Diversification analyses

A likelihood ratio test indicated that a model accounting for one rate

shift was strongly supported against a model without rate shifts

(mean p = 99 Table S21) Models with two or more rate shifts did

not improve model fit Figure 3b shows the mean diversification rate

as a function of time with 80 confidence interval across the 120

trees sampled A diversification rate shift was estimated around

108 Ma (SD = 80) Mean diversification rates were

0012 0014 Ma1 before the rate shift and 015 005 Ma1

after it No significant rate shifts were detected in specific branches

of the MCC tree (Figure S26) and diversification rate in Caribbean

lineages was not significantly different from that of continental

clades (Appendix S2)

Most of the trees simulated with a mass extinction occurring

66 Ma did not display the broom-and-handle shape of the empirical

tree and the crown ages of these trees were younger than the

crown NWTP age (Figure 4a median crown age 47 Ma range of

crown ages 1667ndash191 Ma) The majority of the trees simulated

under a mass extinction 35 Ma displayed the same broom-and-han-

dle shape as our empirical crown NWTP tree (Figure 4b) the crown

age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within

the lower quartile of crown ages of simulated trees which ranged

from 2039 to 218 Ma (median crown age 103 Ma) Most of the

trees simulated with a mass extinction occurring 12 Ma did not dis-

play the broom-and-handle shape of the empirical tree and their

crown ages were older than the crown NWTP age (Figure 4c med-

ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)

4 | DISCUSSION

41 | Divergence times and historical biogeography

411 | Origin of the NWTP in time and space

With all genera and 84 of species sampled our MCC tree (Fig-

ure 2) constitutes the most complete phylogenetic hypothesis

assembled to date for the NWTP Our results are congruent with

CANO ET AL | 5

F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)

6 | CANO ET AL

F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line

CANO ET AL | 7

previous molecular phylogenetic studies and morphological studies

(see Appendix S3 for further discussion) However divergence time

analyses (Figure 2) inferred much older node ages for the stem and

crown of the NWTP (median ages 82 and 77 Ma respectively) and

for the crown of Cryosophileae (45 Ma) than previously estimated

(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning

2016 Figure S27) The use of different taxonomic sampling dating

methods or calibration points could explain those differences Here

however the most likely explanation is our use of the fossil Sabal

bigbendense (Manchester et al 2010) which strongly influenced esti-

mates of divergence times (Figure S11) and which has not previ-

ously been considered in divergence-time analyses of palms We do

not think we placed the fossil calibration incorrectly because our

reassessment of its affinities (Appendix S1) confirmed Manchester

et alrsquos (2010) placement of it in Sabal We predict that the calibrated

molecular dating palm genera by Couvreur et al (2011) would have

estimated older node ages for the NWTP if they had used the fossil

S bigbendense as a node constraint The downstream consequences

of this are minor for the NWTP diversification studies since its bio-

geographical history is here explored for the first time in detail

However further evaluation of S bigbendense as a calibration point

is necessary to assess the biogeography of palms at the global scale

Our biogeographical estimation indicates that the most recent

common ancestor of the NWTP was most probably distributed in

Laurasia (Figure 3a PN = 045) but other geographical origins for

the NWTP were also recovered although with lower relative proba-

bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees

with the scenario posed by Baker and Couvreur (2013a) in which

the origin of the NWTP was inferred to be North America It is

also consistent with fossils of Sabal and Cryosophileae occurring in

a wide range of localities in the Northern Hemisphere including

Europe since the Early Eocene for Sabal and Early Oligocene for

Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De

Franceschi 2012) Taken together these elements indicate that

ancestors of the NWTP were probably a component of the

Boreotropical plant assemblage that covered most of the southern

part of North America and Eurasia during the Palaeocene and early

Eocene (Bjorholm et al 2006)

Our most probable scenario hypothesizes that from North

America Cryosophileae colonized South America where they began

to diversify around 45 Ma (562ndash346 Ma) This dispersal likely

occurred overwater or via stepping stones along the Proto-Antilles

that may have facilitated the Eocene colonization of South America

as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma

Cuenca et al 2008) and other plant groups including Chrysobal-

anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae

492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-

tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend

2011) among others Diversification of Cryosophileae gave rise to

lineages that today occur in subtropical South America (Trithrinax)

and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-

tions deep inland in the tropical rain forest are quite distinct from

those of other Cryosophileae which occur closer to the coast How-

ever during the Miocene a marine incursion prolonged by the

Palaeo-Orinoco fluvial system periodically connected the Western

Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-

amillo et al 2017 Salamanca Villegas et al 2016) We postulate

that this marine incursion and its wetland extensions could have

provided corridors facilitating the propagation of these palms deep

inside South America

412 | Multiple dispersal events to the Caribbeanislands

Our biogeographical reconstruction inferred four dispersal events

from the mainland to the Caribbean islands The most probable sce-

nario had Cryosophileae first dispersing from South America into

North-Central America around 31 Ma (389ndash249 Ma) then into the

Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such

dispersal could have happened overwater as has been inferred for

various groups of animals (eg Fabre et al 2014) and plants (Cer-

vantes et al 2016) Although less likely our reconstruction also

attributed a probability (pNC = 017 pC = 016) to the hypothesis

that the Cryosophileae first colonized the Caribbean islands from

South America during the early Oligocene (Figure 3a) This alterna-

tive dispersal route coincides with the hypothesized GAARlandia

F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers

8 | CANO ET AL

corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed

around the same time although evidence supporting the existence

of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al

2017)

Our results also identify more recent island-mainland exchanges

(Figure 3) Dispersal from North-Central America into the Caribbean

islands during the Pliocene probably gave rise to the Caribbean

endemic clade of Sabal causiarum S domingensis and S maritima

During the same period dispersal events in the opposite direction

were also inferred in Cryosophileae explaining the extant distribution

of Coccothrinax argentata and Thrinax radiata in North-Central Amer-

ica These frequent overwater dispersal events reconstructed for the

NWTP corroborate Baker and Couvreurrsquos (2013a) observation that

long-distance dispersal is a key mechanism underpinning the distri-

bution of palm lineages

42 | Diversification of the NWTP radiation in theCaribbean or mass extinction

We did not find evidence that the diversification rate of the NWTP

in the Caribbean was higher than in continental areas (Appendix S2)

but there was a rate shift across the group as a whole between 137

and 62 Ma (108 Ma Figure 3) Although diversification in Coc-

cothrinax Cryosophila and Sabal increased around that time rate

shifts were not significant in any of these specific lineages (Fig-

ure S26) contradicting a previous diversification analysis that

reported a significant rate shift at the stem node of Coccothrinax

(Baker amp Couvreur 2013b) The difference might be explained by

sampling the latter included only one representative of each genus

with diversification rate derived from species counts whereas we

used a species-level phylogeny but with four of the 14 species

excluded because of missing data Also the rate shift detected by

our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-

structed dispersal of Cryosophileae into the islands rather than con-

temporaneous with colonization Therefore a causal link between

island colonization and increased diversification is rejected for the

NWTP Instead the diversification rate increase coincides temporally

with the mid-Miocene cooling that enhanced the expansion of arid

and semi-arid environments in tropical America (Graham 2010)

Since the greatest diversity of the NTWP is found in dry environ-

ments outside the tropical rain forest (eg Coccothrinax and Sabal)

we hypothesize that the shift to increased seasonality during the

mid-Miocene could have triggered an increase in diversification rate

for the NWTP as in other plant groups such as Cactaceae and

cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp

Morlon 2015)

The wider geographical distribution of the NWTP in the past

than today (Figure 1) and the two particularly long branches (at least

20 and 57 Myr) leading to the crown nodes of Cryosophileae and

Sabaleae (Figure 2) suggest that extinctions could also have

impacted the diversification of these tribes Indeed tree simulations

have demonstrated that broom-and-handle patterns can result from

ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp

Cook 2009) and our simulations indicate that this hypothesis can-

not be rejected for the NWTP The shapes and ages of LTT plots of

trees simulated under a mass extinction at the Terminal Eocene

Event (35 Ma) match most closely those of the NWTP (Figure 4b)

Contrastingly simulations of a mass extinction at the Cretaceousndash

Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did

not show the same pattern crown ages from these simulated mass

extinctions are either too young or too old and show a less evident

broom-and-handle shape (Figure 4ac) These results suggest that the

diversification pattern reconstructed for the NWTP could be related

to a mass extinction event at the Terminal Eocene and a later re-

diversification of the surviving lineages at lower latitudes since the

mid-Miocene The colder conditions at the end of the Eocene could

explain why these elements of the Boreotropical flora were extir-

pated from the northern latitudes (Figure 1 Bjorholm et al 2006)

and may reflect events in other evergreen frost-intolerant taxa that

were once part of the Boreotropical flora but became extinct or

migrated southwards (Jaramillo Rueda amp Mora 2006 Morley

2003) Nevertheless we have not excluded the possibility that a Ter-

minal Eocene extinction event overwrote the signature of an earlier

extinction (eg CretaceousndashPalaeogene) from the diversification pat-

terns recovered for the NWTP

5 | CONCLUSIONS

We identified two main biogeographical explanations for the distri-

bution of the NWTP in the Caribbean region and surrounding land-

masses First a pre-Panama Isthmus colonization of South America

from Laurasia during the Eocene following a dispersal route shared

by other Boreotropical plants (eg Antonelli et al 2009 Bardon

et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a

recolonization of North-Central America around 31 Ma (389ndash

249 Ma) and a subsequent dispersal to the Caribbean islands around

28 Ma (341ndash213) which most probably occurred overwater rather

than through GAARlandia Later overwater dispersal events appear

to have contributed little to the Caribbean species richness of the

NWTP which mainly underwent local diversification We did not

find that island lineages diversified at a higher rate than those on

continents Instead we suggest that the diversification history of

these palms with a long temporal gap from their origin to the begin-

ning of their diversification could reflect the signature of mass

extinction The global climatic cooling at the end of the Eocene

might have had a more significant impact on the diversity and distri-

bution of Caribbean plants

ACKNOWLEDGEMENTS

AC was supported by the International Palm Society Endowment

Fund the Augustin Lombard grant the Commission of the travel

grant and the Foundation Dr Joachim de Giacomi of the Academie

des sciences naturelles Suisse the International Association for Plant

Taxonomy and the Fondation Schmidheiny MP was funded by the

CANO ET AL | 9

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

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Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)

6 | CANO ET AL

F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line

CANO ET AL | 7

previous molecular phylogenetic studies and morphological studies

(see Appendix S3 for further discussion) However divergence time

analyses (Figure 2) inferred much older node ages for the stem and

crown of the NWTP (median ages 82 and 77 Ma respectively) and

for the crown of Cryosophileae (45 Ma) than previously estimated

(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning

2016 Figure S27) The use of different taxonomic sampling dating

methods or calibration points could explain those differences Here

however the most likely explanation is our use of the fossil Sabal

bigbendense (Manchester et al 2010) which strongly influenced esti-

mates of divergence times (Figure S11) and which has not previ-

ously been considered in divergence-time analyses of palms We do

not think we placed the fossil calibration incorrectly because our

reassessment of its affinities (Appendix S1) confirmed Manchester

et alrsquos (2010) placement of it in Sabal We predict that the calibrated

molecular dating palm genera by Couvreur et al (2011) would have

estimated older node ages for the NWTP if they had used the fossil

S bigbendense as a node constraint The downstream consequences

of this are minor for the NWTP diversification studies since its bio-

geographical history is here explored for the first time in detail

However further evaluation of S bigbendense as a calibration point

is necessary to assess the biogeography of palms at the global scale

Our biogeographical estimation indicates that the most recent

common ancestor of the NWTP was most probably distributed in

Laurasia (Figure 3a PN = 045) but other geographical origins for

the NWTP were also recovered although with lower relative proba-

bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees

with the scenario posed by Baker and Couvreur (2013a) in which

the origin of the NWTP was inferred to be North America It is

also consistent with fossils of Sabal and Cryosophileae occurring in

a wide range of localities in the Northern Hemisphere including

Europe since the Early Eocene for Sabal and Early Oligocene for

Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De

Franceschi 2012) Taken together these elements indicate that

ancestors of the NWTP were probably a component of the

Boreotropical plant assemblage that covered most of the southern

part of North America and Eurasia during the Palaeocene and early

Eocene (Bjorholm et al 2006)

Our most probable scenario hypothesizes that from North

America Cryosophileae colonized South America where they began

to diversify around 45 Ma (562ndash346 Ma) This dispersal likely

occurred overwater or via stepping stones along the Proto-Antilles

that may have facilitated the Eocene colonization of South America

as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma

Cuenca et al 2008) and other plant groups including Chrysobal-

anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae

492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-

tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend

2011) among others Diversification of Cryosophileae gave rise to

lineages that today occur in subtropical South America (Trithrinax)

and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-

tions deep inland in the tropical rain forest are quite distinct from

those of other Cryosophileae which occur closer to the coast How-

ever during the Miocene a marine incursion prolonged by the

Palaeo-Orinoco fluvial system periodically connected the Western

Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-

amillo et al 2017 Salamanca Villegas et al 2016) We postulate

that this marine incursion and its wetland extensions could have

provided corridors facilitating the propagation of these palms deep

inside South America

412 | Multiple dispersal events to the Caribbeanislands

Our biogeographical reconstruction inferred four dispersal events

from the mainland to the Caribbean islands The most probable sce-

nario had Cryosophileae first dispersing from South America into

North-Central America around 31 Ma (389ndash249 Ma) then into the

Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such

dispersal could have happened overwater as has been inferred for

various groups of animals (eg Fabre et al 2014) and plants (Cer-

vantes et al 2016) Although less likely our reconstruction also

attributed a probability (pNC = 017 pC = 016) to the hypothesis

that the Cryosophileae first colonized the Caribbean islands from

South America during the early Oligocene (Figure 3a) This alterna-

tive dispersal route coincides with the hypothesized GAARlandia

F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers

8 | CANO ET AL

corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed

around the same time although evidence supporting the existence

of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al

2017)

Our results also identify more recent island-mainland exchanges

(Figure 3) Dispersal from North-Central America into the Caribbean

islands during the Pliocene probably gave rise to the Caribbean

endemic clade of Sabal causiarum S domingensis and S maritima

During the same period dispersal events in the opposite direction

were also inferred in Cryosophileae explaining the extant distribution

of Coccothrinax argentata and Thrinax radiata in North-Central Amer-

ica These frequent overwater dispersal events reconstructed for the

NWTP corroborate Baker and Couvreurrsquos (2013a) observation that

long-distance dispersal is a key mechanism underpinning the distri-

bution of palm lineages

42 | Diversification of the NWTP radiation in theCaribbean or mass extinction

We did not find evidence that the diversification rate of the NWTP

in the Caribbean was higher than in continental areas (Appendix S2)

but there was a rate shift across the group as a whole between 137

and 62 Ma (108 Ma Figure 3) Although diversification in Coc-

cothrinax Cryosophila and Sabal increased around that time rate

shifts were not significant in any of these specific lineages (Fig-

ure S26) contradicting a previous diversification analysis that

reported a significant rate shift at the stem node of Coccothrinax

(Baker amp Couvreur 2013b) The difference might be explained by

sampling the latter included only one representative of each genus

with diversification rate derived from species counts whereas we

used a species-level phylogeny but with four of the 14 species

excluded because of missing data Also the rate shift detected by

our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-

structed dispersal of Cryosophileae into the islands rather than con-

temporaneous with colonization Therefore a causal link between

island colonization and increased diversification is rejected for the

NWTP Instead the diversification rate increase coincides temporally

with the mid-Miocene cooling that enhanced the expansion of arid

and semi-arid environments in tropical America (Graham 2010)

Since the greatest diversity of the NTWP is found in dry environ-

ments outside the tropical rain forest (eg Coccothrinax and Sabal)

we hypothesize that the shift to increased seasonality during the

mid-Miocene could have triggered an increase in diversification rate

for the NWTP as in other plant groups such as Cactaceae and

cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp

Morlon 2015)

The wider geographical distribution of the NWTP in the past

than today (Figure 1) and the two particularly long branches (at least

20 and 57 Myr) leading to the crown nodes of Cryosophileae and

Sabaleae (Figure 2) suggest that extinctions could also have

impacted the diversification of these tribes Indeed tree simulations

have demonstrated that broom-and-handle patterns can result from

ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp

Cook 2009) and our simulations indicate that this hypothesis can-

not be rejected for the NWTP The shapes and ages of LTT plots of

trees simulated under a mass extinction at the Terminal Eocene

Event (35 Ma) match most closely those of the NWTP (Figure 4b)

Contrastingly simulations of a mass extinction at the Cretaceousndash

Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did

not show the same pattern crown ages from these simulated mass

extinctions are either too young or too old and show a less evident

broom-and-handle shape (Figure 4ac) These results suggest that the

diversification pattern reconstructed for the NWTP could be related

to a mass extinction event at the Terminal Eocene and a later re-

diversification of the surviving lineages at lower latitudes since the

mid-Miocene The colder conditions at the end of the Eocene could

explain why these elements of the Boreotropical flora were extir-

pated from the northern latitudes (Figure 1 Bjorholm et al 2006)

and may reflect events in other evergreen frost-intolerant taxa that

were once part of the Boreotropical flora but became extinct or

migrated southwards (Jaramillo Rueda amp Mora 2006 Morley

2003) Nevertheless we have not excluded the possibility that a Ter-

minal Eocene extinction event overwrote the signature of an earlier

extinction (eg CretaceousndashPalaeogene) from the diversification pat-

terns recovered for the NWTP

5 | CONCLUSIONS

We identified two main biogeographical explanations for the distri-

bution of the NWTP in the Caribbean region and surrounding land-

masses First a pre-Panama Isthmus colonization of South America

from Laurasia during the Eocene following a dispersal route shared

by other Boreotropical plants (eg Antonelli et al 2009 Bardon

et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a

recolonization of North-Central America around 31 Ma (389ndash

249 Ma) and a subsequent dispersal to the Caribbean islands around

28 Ma (341ndash213) which most probably occurred overwater rather

than through GAARlandia Later overwater dispersal events appear

to have contributed little to the Caribbean species richness of the

NWTP which mainly underwent local diversification We did not

find that island lineages diversified at a higher rate than those on

continents Instead we suggest that the diversification history of

these palms with a long temporal gap from their origin to the begin-

ning of their diversification could reflect the signature of mass

extinction The global climatic cooling at the end of the Eocene

might have had a more significant impact on the diversity and distri-

bution of Caribbean plants

ACKNOWLEDGEMENTS

AC was supported by the International Palm Society Endowment

Fund the Augustin Lombard grant the Commission of the travel

grant and the Foundation Dr Joachim de Giacomi of the Academie

des sciences naturelles Suisse the International Association for Plant

Taxonomy and the Fondation Schmidheiny MP was funded by the

CANO ET AL | 9

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

REFERENCES

Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line

CANO ET AL | 7

previous molecular phylogenetic studies and morphological studies

(see Appendix S3 for further discussion) However divergence time

analyses (Figure 2) inferred much older node ages for the stem and

crown of the NWTP (median ages 82 and 77 Ma respectively) and

for the crown of Cryosophileae (45 Ma) than previously estimated

(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning

2016 Figure S27) The use of different taxonomic sampling dating

methods or calibration points could explain those differences Here

however the most likely explanation is our use of the fossil Sabal

bigbendense (Manchester et al 2010) which strongly influenced esti-

mates of divergence times (Figure S11) and which has not previ-

ously been considered in divergence-time analyses of palms We do

not think we placed the fossil calibration incorrectly because our

reassessment of its affinities (Appendix S1) confirmed Manchester

et alrsquos (2010) placement of it in Sabal We predict that the calibrated

molecular dating palm genera by Couvreur et al (2011) would have

estimated older node ages for the NWTP if they had used the fossil

S bigbendense as a node constraint The downstream consequences

of this are minor for the NWTP diversification studies since its bio-

geographical history is here explored for the first time in detail

However further evaluation of S bigbendense as a calibration point

is necessary to assess the biogeography of palms at the global scale

Our biogeographical estimation indicates that the most recent

common ancestor of the NWTP was most probably distributed in

Laurasia (Figure 3a PN = 045) but other geographical origins for

the NWTP were also recovered although with lower relative proba-

bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees

with the scenario posed by Baker and Couvreur (2013a) in which

the origin of the NWTP was inferred to be North America It is

also consistent with fossils of Sabal and Cryosophileae occurring in

a wide range of localities in the Northern Hemisphere including

Europe since the Early Eocene for Sabal and Early Oligocene for

Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De

Franceschi 2012) Taken together these elements indicate that

ancestors of the NWTP were probably a component of the

Boreotropical plant assemblage that covered most of the southern

part of North America and Eurasia during the Palaeocene and early

Eocene (Bjorholm et al 2006)

Our most probable scenario hypothesizes that from North

America Cryosophileae colonized South America where they began

to diversify around 45 Ma (562ndash346 Ma) This dispersal likely

occurred overwater or via stepping stones along the Proto-Antilles

that may have facilitated the Eocene colonization of South America

as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma

Cuenca et al 2008) and other plant groups including Chrysobal-

anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae

492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-

tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend

2011) among others Diversification of Cryosophileae gave rise to

lineages that today occur in subtropical South America (Trithrinax)

and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-

tions deep inland in the tropical rain forest are quite distinct from

those of other Cryosophileae which occur closer to the coast How-

ever during the Miocene a marine incursion prolonged by the

Palaeo-Orinoco fluvial system periodically connected the Western

Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-

amillo et al 2017 Salamanca Villegas et al 2016) We postulate

that this marine incursion and its wetland extensions could have

provided corridors facilitating the propagation of these palms deep

inside South America

412 | Multiple dispersal events to the Caribbeanislands

Our biogeographical reconstruction inferred four dispersal events

from the mainland to the Caribbean islands The most probable sce-

nario had Cryosophileae first dispersing from South America into

North-Central America around 31 Ma (389ndash249 Ma) then into the

Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such

dispersal could have happened overwater as has been inferred for

various groups of animals (eg Fabre et al 2014) and plants (Cer-

vantes et al 2016) Although less likely our reconstruction also

attributed a probability (pNC = 017 pC = 016) to the hypothesis

that the Cryosophileae first colonized the Caribbean islands from

South America during the early Oligocene (Figure 3a) This alterna-

tive dispersal route coincides with the hypothesized GAARlandia

F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers

8 | CANO ET AL

corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed

around the same time although evidence supporting the existence

of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al

2017)

Our results also identify more recent island-mainland exchanges

(Figure 3) Dispersal from North-Central America into the Caribbean

islands during the Pliocene probably gave rise to the Caribbean

endemic clade of Sabal causiarum S domingensis and S maritima

During the same period dispersal events in the opposite direction

were also inferred in Cryosophileae explaining the extant distribution

of Coccothrinax argentata and Thrinax radiata in North-Central Amer-

ica These frequent overwater dispersal events reconstructed for the

NWTP corroborate Baker and Couvreurrsquos (2013a) observation that

long-distance dispersal is a key mechanism underpinning the distri-

bution of palm lineages

42 | Diversification of the NWTP radiation in theCaribbean or mass extinction

We did not find evidence that the diversification rate of the NWTP

in the Caribbean was higher than in continental areas (Appendix S2)

but there was a rate shift across the group as a whole between 137

and 62 Ma (108 Ma Figure 3) Although diversification in Coc-

cothrinax Cryosophila and Sabal increased around that time rate

shifts were not significant in any of these specific lineages (Fig-

ure S26) contradicting a previous diversification analysis that

reported a significant rate shift at the stem node of Coccothrinax

(Baker amp Couvreur 2013b) The difference might be explained by

sampling the latter included only one representative of each genus

with diversification rate derived from species counts whereas we

used a species-level phylogeny but with four of the 14 species

excluded because of missing data Also the rate shift detected by

our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-

structed dispersal of Cryosophileae into the islands rather than con-

temporaneous with colonization Therefore a causal link between

island colonization and increased diversification is rejected for the

NWTP Instead the diversification rate increase coincides temporally

with the mid-Miocene cooling that enhanced the expansion of arid

and semi-arid environments in tropical America (Graham 2010)

Since the greatest diversity of the NTWP is found in dry environ-

ments outside the tropical rain forest (eg Coccothrinax and Sabal)

we hypothesize that the shift to increased seasonality during the

mid-Miocene could have triggered an increase in diversification rate

for the NWTP as in other plant groups such as Cactaceae and

cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp

Morlon 2015)

The wider geographical distribution of the NWTP in the past

than today (Figure 1) and the two particularly long branches (at least

20 and 57 Myr) leading to the crown nodes of Cryosophileae and

Sabaleae (Figure 2) suggest that extinctions could also have

impacted the diversification of these tribes Indeed tree simulations

have demonstrated that broom-and-handle patterns can result from

ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp

Cook 2009) and our simulations indicate that this hypothesis can-

not be rejected for the NWTP The shapes and ages of LTT plots of

trees simulated under a mass extinction at the Terminal Eocene

Event (35 Ma) match most closely those of the NWTP (Figure 4b)

Contrastingly simulations of a mass extinction at the Cretaceousndash

Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did

not show the same pattern crown ages from these simulated mass

extinctions are either too young or too old and show a less evident

broom-and-handle shape (Figure 4ac) These results suggest that the

diversification pattern reconstructed for the NWTP could be related

to a mass extinction event at the Terminal Eocene and a later re-

diversification of the surviving lineages at lower latitudes since the

mid-Miocene The colder conditions at the end of the Eocene could

explain why these elements of the Boreotropical flora were extir-

pated from the northern latitudes (Figure 1 Bjorholm et al 2006)

and may reflect events in other evergreen frost-intolerant taxa that

were once part of the Boreotropical flora but became extinct or

migrated southwards (Jaramillo Rueda amp Mora 2006 Morley

2003) Nevertheless we have not excluded the possibility that a Ter-

minal Eocene extinction event overwrote the signature of an earlier

extinction (eg CretaceousndashPalaeogene) from the diversification pat-

terns recovered for the NWTP

5 | CONCLUSIONS

We identified two main biogeographical explanations for the distri-

bution of the NWTP in the Caribbean region and surrounding land-

masses First a pre-Panama Isthmus colonization of South America

from Laurasia during the Eocene following a dispersal route shared

by other Boreotropical plants (eg Antonelli et al 2009 Bardon

et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a

recolonization of North-Central America around 31 Ma (389ndash

249 Ma) and a subsequent dispersal to the Caribbean islands around

28 Ma (341ndash213) which most probably occurred overwater rather

than through GAARlandia Later overwater dispersal events appear

to have contributed little to the Caribbean species richness of the

NWTP which mainly underwent local diversification We did not

find that island lineages diversified at a higher rate than those on

continents Instead we suggest that the diversification history of

these palms with a long temporal gap from their origin to the begin-

ning of their diversification could reflect the signature of mass

extinction The global climatic cooling at the end of the Eocene

might have had a more significant impact on the diversity and distri-

bution of Caribbean plants

ACKNOWLEDGEMENTS

AC was supported by the International Palm Society Endowment

Fund the Augustin Lombard grant the Commission of the travel

grant and the Foundation Dr Joachim de Giacomi of the Academie

des sciences naturelles Suisse the International Association for Plant

Taxonomy and the Fondation Schmidheiny MP was funded by the

CANO ET AL | 9

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

REFERENCES

Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

previous molecular phylogenetic studies and morphological studies

(see Appendix S3 for further discussion) However divergence time

analyses (Figure 2) inferred much older node ages for the stem and

crown of the NWTP (median ages 82 and 77 Ma respectively) and

for the crown of Cryosophileae (45 Ma) than previously estimated

(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning

2016 Figure S27) The use of different taxonomic sampling dating

methods or calibration points could explain those differences Here

however the most likely explanation is our use of the fossil Sabal

bigbendense (Manchester et al 2010) which strongly influenced esti-

mates of divergence times (Figure S11) and which has not previ-

ously been considered in divergence-time analyses of palms We do

not think we placed the fossil calibration incorrectly because our

reassessment of its affinities (Appendix S1) confirmed Manchester

et alrsquos (2010) placement of it in Sabal We predict that the calibrated

molecular dating palm genera by Couvreur et al (2011) would have

estimated older node ages for the NWTP if they had used the fossil

S bigbendense as a node constraint The downstream consequences

of this are minor for the NWTP diversification studies since its bio-

geographical history is here explored for the first time in detail

However further evaluation of S bigbendense as a calibration point

is necessary to assess the biogeography of palms at the global scale

Our biogeographical estimation indicates that the most recent

common ancestor of the NWTP was most probably distributed in

Laurasia (Figure 3a PN = 045) but other geographical origins for

the NWTP were also recovered although with lower relative proba-

bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees

with the scenario posed by Baker and Couvreur (2013a) in which

the origin of the NWTP was inferred to be North America It is

also consistent with fossils of Sabal and Cryosophileae occurring in

a wide range of localities in the Northern Hemisphere including

Europe since the Early Eocene for Sabal and Early Oligocene for

Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De

Franceschi 2012) Taken together these elements indicate that

ancestors of the NWTP were probably a component of the

Boreotropical plant assemblage that covered most of the southern

part of North America and Eurasia during the Palaeocene and early

Eocene (Bjorholm et al 2006)

Our most probable scenario hypothesizes that from North

America Cryosophileae colonized South America where they began

to diversify around 45 Ma (562ndash346 Ma) This dispersal likely

occurred overwater or via stepping stones along the Proto-Antilles

that may have facilitated the Eocene colonization of South America

as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma

Cuenca et al 2008) and other plant groups including Chrysobal-

anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae

492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-

tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend

2011) among others Diversification of Cryosophileae gave rise to

lineages that today occur in subtropical South America (Trithrinax)

and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-

tions deep inland in the tropical rain forest are quite distinct from

those of other Cryosophileae which occur closer to the coast How-

ever during the Miocene a marine incursion prolonged by the

Palaeo-Orinoco fluvial system periodically connected the Western

Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-

amillo et al 2017 Salamanca Villegas et al 2016) We postulate

that this marine incursion and its wetland extensions could have

provided corridors facilitating the propagation of these palms deep

inside South America

412 | Multiple dispersal events to the Caribbeanislands

Our biogeographical reconstruction inferred four dispersal events

from the mainland to the Caribbean islands The most probable sce-

nario had Cryosophileae first dispersing from South America into

North-Central America around 31 Ma (389ndash249 Ma) then into the

Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such

dispersal could have happened overwater as has been inferred for

various groups of animals (eg Fabre et al 2014) and plants (Cer-

vantes et al 2016) Although less likely our reconstruction also

attributed a probability (pNC = 017 pC = 016) to the hypothesis

that the Cryosophileae first colonized the Caribbean islands from

South America during the early Oligocene (Figure 3a) This alterna-

tive dispersal route coincides with the hypothesized GAARlandia

F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers

8 | CANO ET AL

corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed

around the same time although evidence supporting the existence

of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al

2017)

Our results also identify more recent island-mainland exchanges

(Figure 3) Dispersal from North-Central America into the Caribbean

islands during the Pliocene probably gave rise to the Caribbean

endemic clade of Sabal causiarum S domingensis and S maritima

During the same period dispersal events in the opposite direction

were also inferred in Cryosophileae explaining the extant distribution

of Coccothrinax argentata and Thrinax radiata in North-Central Amer-

ica These frequent overwater dispersal events reconstructed for the

NWTP corroborate Baker and Couvreurrsquos (2013a) observation that

long-distance dispersal is a key mechanism underpinning the distri-

bution of palm lineages

42 | Diversification of the NWTP radiation in theCaribbean or mass extinction

We did not find evidence that the diversification rate of the NWTP

in the Caribbean was higher than in continental areas (Appendix S2)

but there was a rate shift across the group as a whole between 137

and 62 Ma (108 Ma Figure 3) Although diversification in Coc-

cothrinax Cryosophila and Sabal increased around that time rate

shifts were not significant in any of these specific lineages (Fig-

ure S26) contradicting a previous diversification analysis that

reported a significant rate shift at the stem node of Coccothrinax

(Baker amp Couvreur 2013b) The difference might be explained by

sampling the latter included only one representative of each genus

with diversification rate derived from species counts whereas we

used a species-level phylogeny but with four of the 14 species

excluded because of missing data Also the rate shift detected by

our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-

structed dispersal of Cryosophileae into the islands rather than con-

temporaneous with colonization Therefore a causal link between

island colonization and increased diversification is rejected for the

NWTP Instead the diversification rate increase coincides temporally

with the mid-Miocene cooling that enhanced the expansion of arid

and semi-arid environments in tropical America (Graham 2010)

Since the greatest diversity of the NTWP is found in dry environ-

ments outside the tropical rain forest (eg Coccothrinax and Sabal)

we hypothesize that the shift to increased seasonality during the

mid-Miocene could have triggered an increase in diversification rate

for the NWTP as in other plant groups such as Cactaceae and

cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp

Morlon 2015)

The wider geographical distribution of the NWTP in the past

than today (Figure 1) and the two particularly long branches (at least

20 and 57 Myr) leading to the crown nodes of Cryosophileae and

Sabaleae (Figure 2) suggest that extinctions could also have

impacted the diversification of these tribes Indeed tree simulations

have demonstrated that broom-and-handle patterns can result from

ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp

Cook 2009) and our simulations indicate that this hypothesis can-

not be rejected for the NWTP The shapes and ages of LTT plots of

trees simulated under a mass extinction at the Terminal Eocene

Event (35 Ma) match most closely those of the NWTP (Figure 4b)

Contrastingly simulations of a mass extinction at the Cretaceousndash

Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did

not show the same pattern crown ages from these simulated mass

extinctions are either too young or too old and show a less evident

broom-and-handle shape (Figure 4ac) These results suggest that the

diversification pattern reconstructed for the NWTP could be related

to a mass extinction event at the Terminal Eocene and a later re-

diversification of the surviving lineages at lower latitudes since the

mid-Miocene The colder conditions at the end of the Eocene could

explain why these elements of the Boreotropical flora were extir-

pated from the northern latitudes (Figure 1 Bjorholm et al 2006)

and may reflect events in other evergreen frost-intolerant taxa that

were once part of the Boreotropical flora but became extinct or

migrated southwards (Jaramillo Rueda amp Mora 2006 Morley

2003) Nevertheless we have not excluded the possibility that a Ter-

minal Eocene extinction event overwrote the signature of an earlier

extinction (eg CretaceousndashPalaeogene) from the diversification pat-

terns recovered for the NWTP

5 | CONCLUSIONS

We identified two main biogeographical explanations for the distri-

bution of the NWTP in the Caribbean region and surrounding land-

masses First a pre-Panama Isthmus colonization of South America

from Laurasia during the Eocene following a dispersal route shared

by other Boreotropical plants (eg Antonelli et al 2009 Bardon

et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a

recolonization of North-Central America around 31 Ma (389ndash

249 Ma) and a subsequent dispersal to the Caribbean islands around

28 Ma (341ndash213) which most probably occurred overwater rather

than through GAARlandia Later overwater dispersal events appear

to have contributed little to the Caribbean species richness of the

NWTP which mainly underwent local diversification We did not

find that island lineages diversified at a higher rate than those on

continents Instead we suggest that the diversification history of

these palms with a long temporal gap from their origin to the begin-

ning of their diversification could reflect the signature of mass

extinction The global climatic cooling at the end of the Eocene

might have had a more significant impact on the diversity and distri-

bution of Caribbean plants

ACKNOWLEDGEMENTS

AC was supported by the International Palm Society Endowment

Fund the Augustin Lombard grant the Commission of the travel

grant and the Foundation Dr Joachim de Giacomi of the Academie

des sciences naturelles Suisse the International Association for Plant

Taxonomy and the Fondation Schmidheiny MP was funded by the

CANO ET AL | 9

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

REFERENCES

Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed

around the same time although evidence supporting the existence

of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al

2017)

Our results also identify more recent island-mainland exchanges

(Figure 3) Dispersal from North-Central America into the Caribbean

islands during the Pliocene probably gave rise to the Caribbean

endemic clade of Sabal causiarum S domingensis and S maritima

During the same period dispersal events in the opposite direction

were also inferred in Cryosophileae explaining the extant distribution

of Coccothrinax argentata and Thrinax radiata in North-Central Amer-

ica These frequent overwater dispersal events reconstructed for the

NWTP corroborate Baker and Couvreurrsquos (2013a) observation that

long-distance dispersal is a key mechanism underpinning the distri-

bution of palm lineages

42 | Diversification of the NWTP radiation in theCaribbean or mass extinction

We did not find evidence that the diversification rate of the NWTP

in the Caribbean was higher than in continental areas (Appendix S2)

but there was a rate shift across the group as a whole between 137

and 62 Ma (108 Ma Figure 3) Although diversification in Coc-

cothrinax Cryosophila and Sabal increased around that time rate

shifts were not significant in any of these specific lineages (Fig-

ure S26) contradicting a previous diversification analysis that

reported a significant rate shift at the stem node of Coccothrinax

(Baker amp Couvreur 2013b) The difference might be explained by

sampling the latter included only one representative of each genus

with diversification rate derived from species counts whereas we

used a species-level phylogeny but with four of the 14 species

excluded because of missing data Also the rate shift detected by

our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-

structed dispersal of Cryosophileae into the islands rather than con-

temporaneous with colonization Therefore a causal link between

island colonization and increased diversification is rejected for the

NWTP Instead the diversification rate increase coincides temporally

with the mid-Miocene cooling that enhanced the expansion of arid

and semi-arid environments in tropical America (Graham 2010)

Since the greatest diversity of the NTWP is found in dry environ-

ments outside the tropical rain forest (eg Coccothrinax and Sabal)

we hypothesize that the shift to increased seasonality during the

mid-Miocene could have triggered an increase in diversification rate

for the NWTP as in other plant groups such as Cactaceae and

cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp

Morlon 2015)

The wider geographical distribution of the NWTP in the past

than today (Figure 1) and the two particularly long branches (at least

20 and 57 Myr) leading to the crown nodes of Cryosophileae and

Sabaleae (Figure 2) suggest that extinctions could also have

impacted the diversification of these tribes Indeed tree simulations

have demonstrated that broom-and-handle patterns can result from

ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp

Cook 2009) and our simulations indicate that this hypothesis can-

not be rejected for the NWTP The shapes and ages of LTT plots of

trees simulated under a mass extinction at the Terminal Eocene

Event (35 Ma) match most closely those of the NWTP (Figure 4b)

Contrastingly simulations of a mass extinction at the Cretaceousndash

Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did

not show the same pattern crown ages from these simulated mass

extinctions are either too young or too old and show a less evident

broom-and-handle shape (Figure 4ac) These results suggest that the

diversification pattern reconstructed for the NWTP could be related

to a mass extinction event at the Terminal Eocene and a later re-

diversification of the surviving lineages at lower latitudes since the

mid-Miocene The colder conditions at the end of the Eocene could

explain why these elements of the Boreotropical flora were extir-

pated from the northern latitudes (Figure 1 Bjorholm et al 2006)

and may reflect events in other evergreen frost-intolerant taxa that

were once part of the Boreotropical flora but became extinct or

migrated southwards (Jaramillo Rueda amp Mora 2006 Morley

2003) Nevertheless we have not excluded the possibility that a Ter-

minal Eocene extinction event overwrote the signature of an earlier

extinction (eg CretaceousndashPalaeogene) from the diversification pat-

terns recovered for the NWTP

5 | CONCLUSIONS

We identified two main biogeographical explanations for the distri-

bution of the NWTP in the Caribbean region and surrounding land-

masses First a pre-Panama Isthmus colonization of South America

from Laurasia during the Eocene following a dispersal route shared

by other Boreotropical plants (eg Antonelli et al 2009 Bardon

et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a

recolonization of North-Central America around 31 Ma (389ndash

249 Ma) and a subsequent dispersal to the Caribbean islands around

28 Ma (341ndash213) which most probably occurred overwater rather

than through GAARlandia Later overwater dispersal events appear

to have contributed little to the Caribbean species richness of the

NWTP which mainly underwent local diversification We did not

find that island lineages diversified at a higher rate than those on

continents Instead we suggest that the diversification history of

these palms with a long temporal gap from their origin to the begin-

ning of their diversification could reflect the signature of mass

extinction The global climatic cooling at the end of the Eocene

might have had a more significant impact on the diversity and distri-

bution of Caribbean plants

ACKNOWLEDGEMENTS

AC was supported by the International Palm Society Endowment

Fund the Augustin Lombard grant the Commission of the travel

grant and the Foundation Dr Joachim de Giacomi of the Academie

des sciences naturelles Suisse the International Association for Plant

Taxonomy and the Fondation Schmidheiny MP was funded by the

CANO ET AL | 9

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

REFERENCES

Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

Swiss National Science Foundation (31003A_1756551) CDB and

AA were funded by the Swedish (B0569601) and European

(331024 FP2007-2013) Research Councils a Wallenberg Academy

Fellowship and the Swedish Foundation for Strategic Research We

thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S

Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and

M Griffiths (FTBG) and R Niba for facilitating samples and data col-

lection and I Sanmartın for her guidance in the simulation analyses

We thank MN Dawson L Cook and J Roncal for their valuable

insights into the manuscript

ORCID

Angela Cano httporcidorg0000-0002-5090-7730

Christine D Bacon httporcidorg0000-0003-2341-2705

REFERENCES

Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and

affinities in the West Indies The Botanical Review 74 5ndash36 httpsd

oiorg101007s12229-008-9000-1

Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge

hypothesis gaining a foothold Commentary Journal of Biogeography

39 431ndash433 httpsdoiorg101111j1365-2699201102674x

Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-

ceedings of the National Academy of Sciences 106 9749ndash9754

httpsdoiorg101073pnas0811421106

Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-

cies in the Neotropics Taxon 60 403ndash414

Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or

rapid radiation Reconstructing the spatiotemporal evolution of the

ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-

cal and simulated approaches Systematic Biology 60 596ndash615

httpsdoiorg101093sysbiosyr062

Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R

M Edwards E J (2011) Contemporaneous and recent radiations

of the worldrsquos major succulent plant lineages Proceedings of the

National Academy of Sciences 108 8379ndash8384 httpsdoiorg10

1073pnas1100628108

Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal

drives island radiations in the palm tribe Trachycarpeae (Arecaceae)

Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio

syr123

Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing

geological models of evolution of the Isthmus of Panama in a phylo-

genetic framework Botanical Journal of the Linnean Society 171

287ndash300 httpsdoiorg101111j1095-8339201201281x

Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp

Antonelli A (2015) Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama Proceedings of the National

Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas

1423853112

Baker W J amp Couvreur T L P (2013a) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages I Historical biogeography Journal of Biogeography 40 274ndash

285

Baker W J amp Couvreur T L P (2013b) Global biogeography and

diversification of palms sheds light on the evolution of tropical lin-

eages II Diversification history and origin of regional assemblages

Journal of Biogeography 40 286ndash298 httpsdoiorg101111j

1365-2699201202794x

Baldwin B G amp Sanderson M J (1998) Age and rate of diversification

of the Hawaiian silversword alliance (Compositae) Proceedings of the

National Academy of Sciences 95 9402ndash9406 httpsdoiorg10

1073pnas95169402

Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp

Chave J (2013) Origin and evolution of Chrysobalanaceae Insights

into the evolution of plants in the Neotropics Botanical Journal of the

Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339

201201289x

Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-

sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-

der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144

21

Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)

Historical legacies in the geographical diversity patterns of New

World palm (Arecaceae) subfamilies Botanical Journal of the Linnean

Society 151 113ndash125 httpsdoiorg101111j1095-83392006

00527x

Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-

cepts for understanding early Cenozoic biogeography Journal of Bio-

geography 41 1036ndash1054 httpsdoiorg101111jbi12310

Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated

extinction rates as a trigger for diversification rate shifts Early

amniotes as a case study Scientific Reports 5 17104 httpsdoiorg

101038srep17104

Cano A Perret M amp Stauffer F W (2013) A revision of the genus

Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136

1ndash53

Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)

Successive arrivals since the Miocene shaped the diversity of the

Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography

43 1773ndash1785 httpsdoiorg101111jbi12790

Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands

acted as refugia and pumps for conifer diversity Cladistics 33 69ndash

92

Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)

Origin and diversification of living cycads A cautionary tale on the

impact of the branching process prior in Bayesian molecular dating

BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-

015-0347-8

Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-

sification patterns of tropical rain forests Inferences from a complete

genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg

1011861741-7007-9-44

Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass

extinction Interpreting signatures in molecular phylogenies Evolution

63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x

Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated

phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-

sal between Africa North and South America Molecular Phylogenetics

and Evolution 46 760ndash775 httpsdoiorg101016jympev2007

10010

Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M

amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-

tion of palms Richmond UK Kew Publishing

Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian

phylogenetics with BEAUti and the BEAST 17 Molecular Biology and

Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075

Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-

any Monographs 46 1ndash70 httpsdoiorg10230725027854

Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E

Douzery E J P amp Orlando L (2014) Rodents of the Caribbean

Origin and diversification of hutias unravelled by next-generation

10 | CANO ET AL

museomics Biology Letters 10 20140266 httpsdoiorg101098

rsbl20140266

Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An

all-evidence species-level supertree for the palms (Arecaceae) Molec-

ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10

1016jympev201603002

Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus

evenly divided between South America and radiations on Cuba and

other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash

11 httpsdoiorg101016jympev201202026

FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-

dependent speciation and extinction rates from incompletely resolved

phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10

1093sysbiosyp067

Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis

C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-

era endemic to the Caribbean Island biodiversity hotspot A review

and a molecular phylogenetic perspective The Botanical Review 73

183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]

20CO2

Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-

ence of reciprocal effects between geographic range evolution and

diversification Systematic Biology 60 451ndash465 httpsdoiorg10

1093sysbiosyr046

Graham A (2003) Historical phytogeography of the Greater Antilles

Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)

055[0357HPOTGA]20CO2

Graham A (2010) Late Cretaceous and Cenozoic History of Latin American

Vegetation and Terrestrial Environments St Louis MO Missouri

Botanical Garden Press

Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-

cal support for a Florida origin of the Cuban oak Journal of Bio-

geography 40 632ndash645 httpsdoiorg101111j1365-26992011

02610x

Henderson A Galeano G amp Bernal R (1995) Field guide to the palms

of the Americas Princeton NJ USA Princeton University Press

Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp

Sevink J Antonelli A (2010) Amazonia through time Andean

uplift climate change landscape evolution and biodiversity Science

330 927ndash931 httpsdoiorg101126science1194585

Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the

Caribbean region Implications for Cenozoic biogeography Bulletin of

the American Museum of Natural History 238 1ndash95

Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S

Wesselingh F P (2017) Miocene flooding events of western

Amazonia Science Advances 3 e1601693 httpsdoiorg101126

sciadv1601693

Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in

the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc

ience1121380

Jordan G amp Goldman N (2012) The effects of alignment error and

alignment filtering on the sitewise detection of positive selection

Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10

1093molbevmsr272

Kass R E amp Raftery A E (1995) Bayes factors Journal of the American

Statistical Association 90 773ndash795 httpsdoiorg101080

01621459199510476572

Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel

method for rapid multiple sequence alignment based on fast Fourier

transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10

1093nargkf436

Losos J B amp Ricklefs R E (2009) Adaptation and diversification on

islands Nature 457 830ndash836 httpsdoiorg101038nature07893

Luebert F Hilger H H amp Weigend M (2011) Diversification in the

Andes Age and origins of South American Heliotropium lineages

(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution

61 90ndash102 httpsdoiorg101016jympev201106001

Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant

diversification Frontiers in Ecology and Evolution 2 1ndash17

Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms

(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-

saurs in the Upper Cretaceous Aguja Formation Big Bend National

Park Texas International Journal of Plant Sciences 171 679ndash689

httpsdoiorg101086653688

Matzke N J (2014) Model selection in historical biogeography reveals

that founder-event speciation is a crucial process in island clades

Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio

syu056

Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES

Science Gateway for inference of large phylogenetic trees In Pro-

ceedings of the gateway computing environments workshop (GCE) New

Orleans USA pp 1-8

Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V

Ni~no H (2015) Middle Miocene closure of the Central American

Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa

2815

Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P

(2016) Critically evaluating the theory and performance of Bayesian

analysis of macroevolutionary mixtures Proceedings of the National

Academy of Sciences of the United States of America 113 9569ndash9574

httpsdoiorg101073pnas1518659113

Morley R J (2003) Interplate dispersal paths for megathermal angios-

perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash

20 httpsdoiorg1010781433-8319-00039

Nee S Holmes E C May R M amp Harvey P H (1994) Extinction

rates can be estimated from molecular phylogenies Phylosophical

Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10

1098rstb19940054

Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-

geography of endemic seed plant genera in the Caribbean Did

GAARlandia play a role Ecology and Evolution 7 10158ndash10174

httpsdoiorg101002ece33521

Nylander J A (2004) MrAICpl Program distributed by the author Upp-

sala Sweden Evolutionary Biology Centre Uppsala University

OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S

A amp Cione A L Jackson J B (2016) Formation of the Isthmus

of Panama Science Advances 2 e1600883 httpsdoiorg101126

sciadv1600883

Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of

threatened seed plant species endemic in the Caribbean Islands The

Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-

9130-y

Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T

(2010) GUIDANCE A web server for assessing alignment confidence

scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10

1093nargkq443

Rabosky D L (2014) Automatic detection of key innovations rate

shifts and diversity-dependence on phylogenetic trees PLoS ONE 9

e89543 httpsdoiorg101371journalpone0089543

Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-

oretical and practical concerns in the analysis of multi-rate diversifi-

cation models Systematic Biology 66 477ndash498 httpsdoiorg10

1093sysbiosyx037

Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer

v16 Retrieved from httpbeastbioedacukTracer

Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-

graphic range evolution by dispersal local extinction and cladogene-

sis Systematic Biology 57 4ndash14 httpsdoiorg101080

10635150701883881

CANO ET AL | 11

Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of

biogeography and evolution Philosophical Transactions of the Royal

Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10

1098rstb20072068

Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies

of Caribbean Palms (Arecaceae) and their relationships to biogeogra-

phy and conservation The Botanical Review 74 78ndash102 httpsdoi

org101007s12229-008-9005-9

Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna

S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-

genetic inference and model choice across a large model space System-

atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029

Rull V (2011) Neotropical biodiversity Timing and potential drivers

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Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R

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BIOSKETCH

Angela Cano is interested in understanding how ecological and

evolutionary processes shape tropical forest biodiversity She is

mainly focused on the Neotropical region and uses palms as a

model to unravel the historical assembly of its flora She con-

ducted her PhD at the University of Geneva and the Botanical

Garden of Geneva in collaboration with the Antonelli Lab at the

University of Gothenburg

Author contributions MP FWS AC AA and CDB con-

ceived the ideas AC and FWS collected the data AC MLS-

S and CDB analysed the data and AC MP CDB AA and

FWS participated in the writing of the manuscript

SUPPORTING INFORMATION

Additional Supporting Information may be found online in the

supporting information tab for this article

How to cite this article Cano A Bacon CD Stauffer FW

Antonelli A Serrano-Serrano ML Perret M The roles of

dispersal and mass extinction in shaping palm diversity across

the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg

101111jbi13225

12 | CANO ET AL

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