on the reversibility of mandibular symphyseal fusion · on the reversibility of mandibular...

ORIGINAL ARTICLE

doi:10.1111/j.1558-5646.2012.01639.x

ON THE REVERSIBILITY OF MANDIBULARSYMPHYSEAL FUSIONJeremiah E. Scott,1 Justin B. Lack,2 and Matthew J. Ravosa3,4,5,6

1Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 465562Department of Zoology, Oklahoma State University, Stillwater, Oklahoma 740783Departments of Biological Sciences, Aerospace and Mechanical Engineering, and Anthropology, University of Notre

Dame, Notre Dame, Indiana 465564Department of Zoology, Mammals Division, Field Museum, Chicago, Illinois 606055Department of Anatomy and Cell Biology, Indiana University School of Medicine–South Bend, South Bend, Indiana 46617

6E-mail: [email protected]

Received October 21, 2011

Accepted March 9, 2012

Experimental and comparative studies suggest that a major determinant of increased ossification of the mandibular symphysis is

elevated masticatory stress related to a mechanically challenging diet. However, the morphology of this joint tracks variation in

dietary properties in only some mammalian clades. Extant anthropoid primates are a notable exception: synostosis is ubiquitous

in this speciose group, despite its great age and diverse array of feeding adaptations. One possible explanation for this pattern is

that, once synostosis evolves, reversion to a lesser degree of fusion is unlikely or even constrained. If correct, this has important

implications for functional and phylogenetic analyses of the mammalian feeding apparatus. To test this hypothesis, we gener-

ated a molecular tree for 76 vespertilionoid and noctilionoid chiropterans using Bayesian phylogenetic analysis and examined

character evolution using parsimony and likelihood ancestral-state reconstructions along with the binary state speciation and

extinction (BiSSE) model. Results indicate that reversals have occurred within Vespertilionoidea. In contrast, noctilionoids exhibit

an anthropoid-like pattern, which suggests that more detailed comparisons of the functional and developmental bases for fusion

in these bat clades may provide insight into why fusion is maintained in some lineages but not in others. Potential functional and

developmental explanations for the lack of reversal are discussed.

KEY WORDS: Chiroptera, constraint, irreversibility, mammals, mandible, Primates, symphysis.

Linking morphological diversity to differences in ecology and

environment among species is one of the primary goals of evo-

lutionary biology. The most common way in which hypotheses

of adaptation are tested is the comparative method (e.g., Kay

and Cartmill 1977; Ridley 1983; Coddington 1988, 1994; Baum

and Larson 1991; Brooks and McLennan 1991; Harvey and Pagel

1991; Losos and Miles 1994; Lauder 1995; Doughty 1996; Larson

and Losos 1996). Using this approach, an interspecific associa-

tion between a trait and an ecological or environmental condition

is interpreted as evidence that the trait is an adaptation—that is,

shaped by natural selection for its current biological role (Bock

and von Wahlert 1965; Williams 1966; Gould and Vrba 1982).

However, identifying the adaptive basis for a given trait is com-

plicated by the existence of factors that may cause the strength

of a trait’s association with its hypothesized selective regime to

vary among clades, with some taxa providing clear support for an

adaptationist hypothesis and others providing no support. Such

factors, typically referred to as constraints, include multivariate

genetic correlations, insufficient genetic variation, and strong in-

ternal selection related to developmental or functional integration

(e.g., Gould and Lewontin 1979; Cheverud 1984; Maynard Smith

et al. 1985; McKitrick 1993; Losos and Miles 1994; Schwenk

1995; Wagner and Schwenk 2000; Futuyma 2010). Constraints

can obscure an interspecific relationship between a trait and its

2 9 4 0C© 2012 The Author(s). Evolution C© 2012 The Society for the Study of Evolution.Evolution 66-9: 2940–2952

IS MANDIBULAR SYMPHYSEAL FUSION REVERSIBLE?

A B C D

Figure 1. Diagrammatic representations of symphyseal character

states in transverse cross section (anterior is up): (A) unfused—

smooth, opposing dentaries loosely connected by fibrous tissue,

a fibrocartilage pad, and ligaments (amphiarthrosis); (B) simple

and (C) complex partial fusion—a continuum of increasingly more

tightly bound joints with greater sutural complexity consisting of

interlocking rugosities and numerous variably calcified ligaments

(synarthrosis); (D) a fully ossified, or fused, joint (synostosis). See

also Scapino (1981).

proposed determinant in at least two ways: (1) by predisposing

homologous traits in different taxa to respond to the same en-

vironmental selective regime (i.e., external selection) in distinct

ways or (2) by opposing such selection pressures. In both of these

cases, the constraint results in the absence of an anticipated evo-

lutionary outcome in some clades (Maynard Smith et al. 1985;

McKitrick 1993).

Within the order Primates, complete ossification, or fusion,

of the mandibular symphyseal joint (i.e., the joint between the

left and right hemimandibles, or dentaries) may represent an ex-

ample of a character that is evolutionarily constrained (Ravosa

1999; Lockwood 2007). Whereas the first primates were char-

acterized by unfused joints with smooth symphyseal plates (e.g.

Fig. 1A), fusion is a synapomorphy of all living and fossil mem-

bers of the crown anthropoid radiation (Kay et al. 1997; Ravosa

1999; Williams et al. 2010; but see Simons and Rasmussen 1996;

Seiffert et al. 2004; Simons 2004), the highly speciose clade com-

prising living and extinct New and Old World monkeys, apes, and

humans (approximately 280 species in 45 genera; Groves 2005).

Fusion has also evolved in fossil strepsirrhine primates (relatives

of extant lemurs, lorises, and galagos), including multiple times in

Eocene adapids and the recently extinct (subfossil) giant lemurs

of Madagascar, as well as convergently in at least one group of

Oligocene stem anthropoids (species closely related to but out-

side of the crown anthropoid clade) (Beecher 1983; Ravosa 1991;

Doughty 1996; Dumont 1999; Ravosa and Hylander 1994; Ravosa

and Simons 1994). In contrast, decreases in ossification have yet

to be documented in primates (Ravosa 1996, 1999). The absence

of reversals in crown anthropoids is particularly notable, given

the great age of this clade (>35 Ma; e.g., Hodgson et al. 2009;

Jameson et al. 2011) and its diverse array of feeding adaptations

(e.g., Rosenberger 1992).

On the other hand, variation in symphyseal fusion in ex-

tant strepsirrhine primates tracks interspecific differences in di-

etary mechanical properties, ranging from unfused with relatively

smooth symphyseal plates in species that feed on relatively easy-

to-process foods, such as insects, ripe fruits, and exudates, to par-

tially fused with complex, interlocking rugosities (e.g., Fig. 1C)

in species that rely on more resistant foods, such as seeds and

leaves (Beecher 1977a,b, 1979; Ravosa 1991; Ravosa and Hylan-

der 1994; Scott et al. 2012). Moreover, complete fusion charac-

terizes giant subfossil lemurs that are inferred, based on studies of

dental wear and morphology (i.e., independently of mandibular

form), to have been seed-predators or dedicated folivores (Jungers

et al. 2002; Rafferty et al. 2002; Godfrey et al. 2004; Scott et al.

2009). The strepsirrhine pattern thus indicates that, in at least

some primates, fusion is an adaptive response to elevated joint

stresses associated with processing a mechanically demanding

diet (Beecher 1977a,b, 1979; Ravosa 1991, 1999; Ravosa and

Hylander 1994; Ravosa and Hogue 2004), and data from other

mammalian clades support this idea (Scott et al. 2012). Given the

fact that anthropoids are as dietarily diverse as strepsirrhines, these

observations suggest that all crown anthropoids have a fused sym-

physis simply because they inherited it from a common ancestor

with a diet composed of items that required intensive postcanine

processing (Ravosa and Hylander 1994; Ravosa 1999). In other

words, symphyseal fusion may have been adaptive at one point

early in the history of this clade but is now retained for reasons

other than selection related to dietary properties (e.g., develop-

mental canalization or functional integration; Lockwood 2007).

Notably, the issues raised above are not limited to pri-

mates. Mammalian clades in which at least some members are

characterized by loss of the symphyseal joint include marsupi-

als, xenarthrans, carnivorans, cetartiodactyls, perissodactyls, pro-

boscideans, hyracoids, and chiropterans (Beecher 1977a,b, 1979;

Scapino 1981; Hogue and Ravosa 2001; Hogue 2004; Ravosa

and Hogue 2004; Williams et al. 2008; Davis et al. 2010; Scott

et al. 2012). Thus, the possibility that the mandibular symph-

ysis is unlikely to become unfused once complete ossification is

achieved has important implications with respect to understanding

the evolution of the masticatory system and testing phylogenetic

hypotheses in a variety of mammalian groups.

Although the contrast between the patterns exhibited by

strepsirrhines and crown anthropoids suggests the existence of

a constraint in the latter group, the fact that complete fusion (as

opposed to partial fusion) is relatively uncommon in strepsirrhines

raises questions about the appropriateness of this comparison—

that is, because fusion is observed in only a handful of extinct

strepsirrhines, and these species are apomorphic for this charac-

ter in comparison to their sister taxa, the Strepsirrhini may not

represent a suitable null model for generating expectations re-

garding the pattern of symphyseal character-state evolution in

crown anthropoids (Schwenk 1995), within which fusion is ple-

siomorphic. Thus, in this study, we examine the evolution of

symphyseal form in the Chiroptera, a clade that may be a bet-

ter analogue in terms of evaluating the anthropoid pattern and

EVOLUTION SEPTEMBER 2012 2 9 4 1

JEREMIAH E. SCOTT ET AL.

addressing questions regarding constraints on symphyseal evolu-

tion in mammals. Although chiropterans are much more distantly

related to the Anthropoidea than are the Strepsirrhini, complete

symphyseal ossification is common in this highly speciose clade

without being ubiquitous, which allows us to test the hypoth-

esis that this condition is irreversible. Moreover, chiropterans,

like anthropoids, are very ecologically diverse. Dietary variation

ranges from widespread insectivory in the Vespertilionidae to the

existence of at least six distinct feeding guilds in Phyllostomi-

dae, including sanguinivory, nectarivory, frugivory, insectivory,

carnivory, and omnivory. Moreover, the diversity in chiropteran

ecology is reflected in the morphology of the masticatory appara-

tus (e.g., Freeman 1979, 1988, 1995; Dumont 1999, 2004; Davis

et al. 2010; Dumont et al. 2012). Examining a more distantly

related clade also allows us to evaluate the generality of the an-

thropoid pattern: is the lack of reversal in the Anthropoidea due

to clade-specific factors? Or is reversal unlikely to occur in any

clade in which symphyseal fusion evolves?

Materials and MethodsSAMPLE

Our sample consisted of 76 taxa from two superfamilies, the

Vespertilionoidea and the Noctilionoidea (Table 1), which are sis-

ter clades within the suborder Yangochiroptera (Teeling et al.

2005; also referred to as Vespertilioniformes; Hutcheon and

Kirsch 2004). Over half of the sample (n = 44) was provided by

R. Beecher, who examined all mammalian genera housed in the

collections of the Smithsonian Institution as part of his disser-

tation research (Beecher 1977b). In several instances, Beecher’s

notes (pers. comm.) list only generic names, and it is not clear

whether such entries are for only a single species or multiple

species within a genus. Thus, n = 76 may be a conservative es-

timate of the number of species included in our analysis. Sample

sizes for Beecher’s taxa are not listed, but he did record intrataxo-

nomic (either intraspecific or intrageneric) variation in some cases

(see the entries for Tadarida, Mormopterus, and Eumops in Table

1). Data for the remaining 32 species in our sample were collected

by MJR at the Field Museum of Natural History. These species

were scored using a four-state system: (1) unfused with smooth

symphyseal plates, (2) partially fused with simple rugosities (sim-

ple partial fusion), (3) partially fused with complex, interlocking

rugosities (complex partial fusion), and (4) fully ossified with no

intraspecific variation (Fig. 1; see also Scapino 1981). The infor-

mation available in Beecher’s notes allowed us to reconcile his

morphological descriptions with our scoring system. Prior to anal-

ysis, the first three character states were collapsed into a single

state, which we refer to hereafter as unfused; thus, species were

ultimately coded as follows: unfused, partially fused, or variably

partially or fully fused = 0; full fusion, with no intraspecific

variation = 1.

PHYLOGENETIC ANALYSIS

Previous phylogenetic analyses of bats have been able to resolve

the majority of relationships within Noctilionoidea, whereas rel-

atively large datasets have been unable to resolve most of the in-

tertribal relationships within Vespertilionoidea (Hoofer and Van

Den Bussche 2003; Lack and Van Den Bussche 2010; Roehrs

et al. 2010). To account for this uncertainty, we obtained from

GenBank an approximately 2.6 kilobase fragment spanning the

12S rRNA, tRNAVAL, and 16S rRNA genes of the mitochondrial

DNA (mtDNA) genome for all chiropteran taxa examined in this

study. GenBank accession numbers are given in Table S1. Se-

quences were aligned using the Geneious aligner (Drummond

et al. 2010) and edited in MacClade (Maddison and Maddison

2002). Any position for which positional homology was ques-

tionable was excluded from further analysis, resulting in 1,988

analyzed positions (898 excluded positions).

We conducted a Bayesian phylogenetic analysis with BEAST

(Drummond and Rambaut 2007) using a relaxed lognormal clock,

a Yule speciation tree prior, and a GTR + I + � model of nu-

cleotide substitution, as suggested by MrModeltest (Nylander

2004). Two internal fossil calibrations were used (with lognormal

priors) to obtain branch lengths in absolute time. The first was a

prior minimum age of 30 million years ago (Ma) for the Phyl-

lostomidae. The oldest probable stem phyllostomids are found in

the Whitneyan (30–32 Ma; Czaplewski et al. 2008). Therefore,

the offset for the lognormal prior was set at 30 Ma with the upper

bound for the 95% quantiles set to the Eocene–Oligocene bound-

ary (34 Ma). The second calibration was a minimum of 37 Ma

for the split between Vespertilionidae and Molossidae, because

verified vespertilionid and molossid fossils have been found from

middle Eocene deposits (McKenna and Bell 1997). The upper

bound of the 95% quantiles was set at 48 Ma to encapsulate the

entire middle Eocene in the prior.

An initial analysis of 50,000,000 generations with 10% burn-

in was run to tune operators. The final analysis consisted of

two separate runs of 50,000,000 generations, each with 10%

burn-in. Results of these final two runs were combined using

LogCombiner—a component of the BEAST package—to obtain

the maximum clade credibility topology. All runs were checked

for sufficient mixing, stable convergence on a unimodal posterior,

and effective sample sizes (Drummond et al. 2002) greater than

200 for all parameters using TRACER (Drummond and Rambaut

2003). The maximum clade credibility tree in Newick format, with

branch lengths in millions of years, is presented in Appendix S1.

We also obtained 1,000 trees from the posterior sample of the

BEAST analysis to incorporate uncertainty in vespertilionoid phy-

logenetic relationships into our analysis. This analytical step was

2 9 4 2 EVOLUTION SEPTEMBER 2012


Table 1. Samples and data used in this study. Taxa that lack a sample size, indicated by a dash (—), were provided by R. Beecher; in many

cases, only genus names are available for this portion of the dataset. Fusion scores are as follows: 1 = unfused, with smooth surfaces;

2 = partially fused, with simple rugosities; 3 = partially fused, with complex, interlocking rugosities; 4 = fully fused.

Taxon n Fusion Taxon n Fusion

NOCTILIONOIDEA Molossidae (continued)Phyllostomidae Promops – 4

Sphaeronycteris toxophyllum – 4 Molossus – 4Pygoderma bilabiatum – 4 Mormopterus – 1,4Centurio senex – 4 MiniopteridaeArdops nichollsi – 4 Miniopterus – 1Artibeus – 4 VespertilionidaeEctophylla alba – 4 Murina – 4Vampyrodes caraccioli – 4 Harpiocephalus – 4Rhinophylla – 4 Kerivoula – 1Carollia – 4 Myotis lucifugus – 1Lionycteris spurrelli 4 4 Myotis macrotarsus – 1Lonchophylla modax 4 4 Myotis vivesi – 2Phylloderma stenops 4 4 Scotophilus – 4Phyllostomus discolor 4 4 Corynorhinus rafinesquii 3 1Mimon cozumelae 4 4 Antrozous pallidus – 4Tonatia bidens 4 4 Rhogessa – 4Trachops cirrhosus 4 4 Lasiurus – 4Macrophyllum macrophyllum 4 4 Idionycteris phyllotis 3 1Vampyrum spectrum 4 4 Euderma maculatum 1 1Chrotopterus auritus 4 4 Otonycteris hemprichii – 4Anoura caudifer 4 4 Barbestella – 4Choeroniscus minor 4 4 Plecotus – 4Choeronycteris mexicana 4 4 Scotomanes ornatus – 4Brachyphylla – 4 Arielulus circumdatus 1 1Erophylla – 4 Eptesicus diminutus 4 1Desmodus rotundus – 3 Eptesicus fuscus 4 4Diaemus youngi – 3 Glauconycteris beatrix 4 1Diphylla ecaudata – 4 Nycticeius – 1Micronycteris megalotis 4 4 Lasionycteris noctivagans – 4Macrotus waterhousii 4 1 Nycticeinops schlieffeni 4 4

Noctilionidae Neoromicia rendalli 3 1Noctilio albiventris 4 4 Laephotis botswanae 1 1Noctilio leporinus 4 4 Nyctophilus – 4

Furipteridae Chalinolobus – 4Furipterus horrens – 1 Vespadelus regulus 2 4

VESPERTILIONOIDEA Hypsugo savii 3 1Natalidae Tylonycteris – 4

Natalus – 1 Vespertilio – 1Chilonatalus – 1 Pipistrellus javanicus 2 4

Molossidae Pipistrellus coromandra 2 1Tadarida – 1, 4 Nyctalus – 4Eumops – 1, 4 Scotoecus hirundo 4 4

accomplished by taking the combined tree file (100,000 trees prior

to burn-in), discarding the first 50% as burn-in (50,000 phyloge-

nies), and using LogCombiner to resample this tree file at a lower

frequency.

Character EvolutionTo test the hypothesis that fusion is irreversible in these two

chiropteran clades, we initially examined patterns of character-

state evolution using Mesquite’s (Maddison and Maddison 2011)



parsimony and maximum likelihood options to map character

states onto the maximum clade credibility tree, with each super-

family being examined separately. Maximum-likelihood recon-

structions were performed using Mesquite’s AsymmMk model

(also referred to as Mk2), which estimates separate rates for each

character-state transition—that is, unfused to fused, and fused to

unfused. We estimated support for likelihood reconstructions at

each node using a decision threshold of T = 2 (Mesquite’s de-

fault). This statistic is the difference between the log-likelihoods

for each character state at the node in question. If this difference

exceeds the threshold, then the state with the higher likelihood

is considered better supported; otherwise, the reconstruction is

considered ambiguous.

Ancestral-state reconstructions based on parsimony and the

AsymmMk maximum-likelihood model can be problematic be-

cause they assume that net diversification rate (i.e., speciation rate

minus extinction rate) is independent of the state of the charac-

ter under study (Cunningham 1999; Goldberg and Igic 2008). If

this assumption does not hold, then reconstructions of ancestral

states for a given character will be biased, leading to incorrect re-

jections of irreversibility (Cunningham 1999; Goldberg and Igic

2008). For example, if organisms with fused symphyses diversify

more rapidly than those with unfused symphyses, then fusion will

eventually be much more common in a phylogeny, and species

with unfused symphyses will appear to have evolved from an an-

cestor with a fused symphysis even if the transition did not in fact

occur.

This issue can be overcome by using methods that incorporate

information regarding the effect of character states on diversifi-

cation rates (Goldberg and Igic 2008). Following recent studies

(Goldberg and Igic 2008; Lynch and Wagner 2010; Kohlsdorf

et al. 2010; Wiens 2011), we used one such approach—Maddison

et al.’s (2007; see also FitzJohn et al. 2009) binary state spe-

ciation and extinction (BiSSE) model—to further evaluate the

irreversibility hypothesis in vespertilionoids and noctilionoids.

BiSSE computes the likelihood for a model with up to six esti-

mated parameters: a speciation rate under each character state (λ0

and λ1), an extinction rate under each character state (μ0 and μ1),

and transition rates from each character state to the other (q01 and

q10) (Maddison et al. 2007). Different models of evolution can

be constructed by fixing one or more of these parameters, and

these models can be compared to each other to determine which

provides the best fit.

We compared four such models. The first of these was the

unconstrained model, in which all six parameters were estimated

using maximum likelihood. Support for this model indicates

that fusion is reversible and that net diversification rates for the

two character states differ. The second model was the equal-

diversification model, in which the net diversification rates for

the two character states were set equal to each other—that is,

λF = λU and μF = μU, so that λF − μF = λU − μU, where

the subscripts F and U denote fused and unfused joints, respec-

tively. Support for this model indicates that fusion is reversible

and that character state does not affect diversification rate. The

third model was the irreversible model, in which the transition

rate from a fused joint to an unfused joint (qFU) was set equal to

zero. Support for this model indicates that reversals have not oc-

curred and that net diversification rates for the two character states

differ. The final model was the irreversible, equal-diversification

model, which prohibits reversal (as in the irreversible model) and

equalizes net diversification rates for the two character states (as

in the equal-diversification model). Support for this model indi-

cates that reversals have not occurred and that net diversification

rates for the two character states do not differ.

We applied FitzJohn et al.’s (2009) correction for incom-

plete sampling of taxonomic diversity. Our samples consisted

of 32 of 177 noctilionoid species and 44 of 515 vespertilionoid

species, representing 72 of the 130 genera recognized by Sim-

mons (2005) in these two superfamilies. All BiSSE computations

were conducted using the program diversitree (FitzJohn 2011) in

R (R Development Core Team 2011). We compared models using

Akaike’s information criterion with adjustment for small sample

size (AICc; Burnham and Anderson 2002). Using this approach,

the relevant statistic is �AICc, which is the difference between

the AICc values for a given model and the model with the lowest

AICc. The model with the lowest AICc value (�AICc = 0.0) is

the best supported. For models with nonzero �AICc values, we

used the following rule of thumb (Burnham and Anderson 2002,

p. 70): �AICc = 0–2 indicates substantial support for the model,

�AICc = 4–7 indicates considerably less support, �AICc > 10

indicates essentially no support.

ResultsVESPERTILIONOIDEA

The parsimony-based character-state reconstructions indicate the

presence of at least seven reversals in the vespertilionoid max-

imum clade credibility tree (Fig. 2). The unfused symphysis of

Corynorhinus rafinesquii may also represent a reversal, but this

case is uncertain due to ambiguity in reconstructions at two deeper

nodes. In contrast, there are no unequivocal instances of reversal

when character states are reconstructed using AsymmMk maxi-

mum likelihood (Fig. 2). Under this approach, the reconstructions

at nearly all of the internal nodes are ambiguous; one state is

judged better than the other (i.e., the likelihood decision thresh-

old is exceeded) at only two of these nodes: in the ancestor of

Promops and Molossus (fused), and in the ancestor of Natalus

and Chilonatalus (unfused; note that the latter two genera have

been collapsed into the family Natalidae in Fig. 2). The highest



45.7 Ma

42.6 Ma

41.2 Ma

32.7 Ma

30.0 Ma

28.7 Ma

28.1 Ma

26.3 Ma

24.2 Ma

Natalidae

Miniopterus

Scotophilus

HarpiocephalusKerivoulaMyotis

Murina

NycticeiusLasionycteris noctivagans

Tylonycteris

ChalinolobusVespadelus regulusHypsugo savii

Nycticeinops schlieffeniNeoromicia rendalliLaephotis botswanae

Vespertilio

Scotoecus hirundoNyctalus

Pipistrellus javanicusP. coromandra

Arielulus circumdatus

Lasiurus

Idionycteris phyllotisEuderma maculatum

Plecotus

Otonycteris hemprichiiBarbastella

Corynorhinus rafinesquii

Antrozous pallidusRhogessa

Scotomanes ornatusEptesicus diminutusE. fuscus

Glauconycteris beatrix

TadaridaEumopsPromopsMolossusMormopterus

Nyctophilus

Figure 2. Maximum clade credibility tree for the Vespertilionoidea showing parsimony-based (left) and likelihood-based (right) ancestral-

state reconstructions: white circle = unfused, partially fused, or variable; black circle = fully fused; black-and-white circle = equivocal

ancestral-state reconstruction (pie charts show the relative likelihood for each character state). The gray rectangles indicate positions

where reversals are inferred to have occurred. Branch lengths are not to scale, but ages of selected internal nodes are given in millions of

years (Ma). Not all 44 taxa included in the analysis are shown; in some cases, clades that are homogeneous with respect to symphyseal

morphology have been collapsed.

relative likelihood of fusion at an ancestral node that has at least

one descendent with an unfused symphysis is 0.696 (the ances-

tor of Nyctalus and Pipistrellis). For comparison, the relative

likelihoods of the states that characterize the Promops–Molossus

and Natalus–Chilonatalus ancestors are 0.887 and 0.934, respec-

tively, and the highest relative likelihood of a state at a node with

an ambiguous reconstruction is 0.830 (fusion in the ancestor of

Nyctophilus and Chalinolobus).

The results of the BiSSE analysis of the Vespertilionoidea

are presented in Table 2. The equal-diversification model receives

the highest support, but the unconstrained model has a very low

�AICc value, indicating that these two models are essentially

indistinguishable from each other. We are therefore unable to

choose between character-independent and character-dependent

diversification, and thus the latter remains a possibility, along with

its potentially confounding effects. (The parameter estimates for

the unconstrained model indicate that lineages characterized by

fusion diversify at rate that is nearly 3.5 times greater than that

for lineages without fusion.) Given this ambiguity, the BiSSE

model is clearly more appropriate than parsimony and likelihood

reconstructions for evaluating the reversibility of symphyseal fu-

sion in vespertilionoids. The BiSSE results nevertheless confirm

the signal obtained using parsimony reconstructions: the two ir-

reversible models have �AICc values that are greater than four

(Table 2), indicating that support for the models that allow rever-

sal is considerably greater. This result is robust to uncertainty

regarding the phylogenetic relationships within our vespertil-

ionoid sample. Figure 3 shows the distribution of �AICc val-

ues for the irreversible model as compared to the unconstrained

model computed for the 1000 topologies from the posterior

sample of the Bayesian phylogenetic analysis. The irreversible

model never has a lower AICc value than the unconstrained



Table 2. Comparison of BiSSE models. The parameters are as follows: λU and λF are the speciation rates for lineages with unfused

and fused symphyses, respectively; μU and μF are the extinction rates; and qUF and qFU are the unfused-to-fused and fused-to-unfused

transition rates, respectively. Dashes (–) indicate that the parameter was fixed (i.e., for equal diversification, λU = λF and μU = μF; for

irreversible, qFU = 0). The final three columns give the log-likelihoods (ln L) for each model and the difference between each model’s AICc

value and minimum observed AICc value (�AICc). The model with the minimum �AICc (in bold) is the best supported.

BiSSE parameters

Model λU λF μU μF qUF qFU ln L �AICc

VESPERTIOLIONOIDEAUnconstrained 0.0511 0.1775 2.3×10−5 1.5×10−5 0.0132 0.0729 −186.44 0.0962Equal diversification 0.1339 – 8.4×10−8 – 0.0517 0.0529 −189.01 0.0000Irreversible 0.1875 0.0221 1.4×10−7 0.0422 0.0928 – −190.07 4.6565Irreversible, equal diversification 0.1338 – 2.0×10−6 – 0.0267 – −192.62 4.7872

NOCTILIONOIDEAUnconstrained 0.0742 0.1435 4.1×10−6 3.5×10−5 0.0181 8.4×10−7 −117.81 3.0539Equal diversification 0.1210 – 6.3×10−8 – 0.0252 5.3×10−10 −120.57 2.6840Irreversible 0.0742 0.1435 9.9×10−7 5.4×10−8 0.0181 – −117.81 0.0000Irreversible, equal diversification 0.1210 – 7.3×10−6 – 0.0256 – −120.57 0.0607

0

20

40

60

80

100

120

-1 0 1 2 3 4 5 6 7 8 9 10 11 12

AICc

Cou

nt

Considerably less support for irreversibility

Substantial support for

irreversibility

∆AICc for irreversible model

Figure 3. Histogram showing the distribution of BiSSE-derived

�AICc values (irreversible AICc minus unconstrained AICc) for the

1000 topologies from the posterior sample of the Bayesian phy-

logenetic analysis. The white arrow indicates the position of the

maximum clade credibility tree.

model (which in this figure would be indicated by a negative

�AICc); moreover, 98.5% of the trees have a �AICc value greater

than two, and 77.9% of trees have a �AICc value greater than

four. These results indicate that at least some vespertilionoids

with unfused symphyses are descended from ancestors with fused

symphyses.

NOCTILIONOIDEA

The distribution of character states in noctilionoids presents a

striking contrast to that exhibited by vespertilionoids. Whereas

the fused and unfused symphyses are equally common in the lat-

ter clade, 28 of the 32 noctilionoids in our sample are characterized

by fusion. Such a distinction might be expected if diversification

of the Noctilionoidea began much later in comparison to vesper-

tilionoids, but this is not the case (compare divergence dates in

Figs. 2 and 4). For example, the least inclusive clade that contains

both Sphaeronycteris and Erophylla is over 20 million years old

and contains 24 taxa, all with complete symphyseal ossification

(Fig. 4). On the other hand, vespertilionoid clades of similar age

are much more morphologically diverse (e.g., the least inclusive

clade containing Nycticeius and Scotoecus; Fig. 2).

Parsimony reconstructions suggest that the unfused symph-

ysis inferred in the last common ancestor of Desmodus rotun-

dus and Diaemus youngi is an instance of reversal (Fig. 4). The

other two noctilionoids with unfused symphyses—Macrotus wa-

terhousii and Furipterus horrens—may also be descended from

ancestors with fused symphyses, but the parsimony reconstruc-

tions at the relevant internal nodes are equivocal. Uncertainty in

the likelihood reconstructions does not allow identification of any

instances of reversal (Fig. 4).

The BiSSE results for this clade indicate that the irre-

versible model is the best supported, with the irreversible, equal-

diversification model being nearly as well supported (Table 2).

Thus, as in the case of the Vespertilionoidea, neither character-

dependent nor character-independent diversification provides a

better fit to our dataset. Moreover, although the �AICc values for

the two models that allow reversal (the unconstrained and equal-

diversification models) are greater than two, they are less than

four, the threshold at which support for a model is regarded as

considerably less (Burnham and Anderson 2002). In other words,

these results do not provide strong support for irreversibility over

reversibility in this superfamily. Our data therefore do not allow

us to claim with confidence that reversals have not occurred in

this clade. Note that because the phylogenetic relationships de-

picted in the noctilionoid maximum clade credibility are robust

(i.e., there is little variation in these relationships from tree to

tree in the posterior sample), we do not present a distribution of

�AICc values as we did for the Vespertilionoidea.



40.6 Ma

31.8 Ma

29.6 Ma

26.7 Ma

23.8 Ma

23.3 Ma

Desmodus rotundus

Diphylla ecaudata

BrachyphyllaErophylla

Diaemus youngi

Furipterus horrensNoctilio leporinusNoctilio albiventris

Anoura caudiferChoeroniscus minorChoeronycteris mexicana

Macrotus waterhousiiMicronycteris megalotis

Chrotopterus auritus

Phyllostomus discolor

Sphaeronycteris toxophyllum

Rhinophylla

Pygoderma bilabiatumCenturio senexArdops nichollsiArtibeusEctophylla albaVampyrodes caraccioli

Carollia

Trachops cirrhosus

Vampyrum spectrum

Tonatia bidens

Lionycteris spurrelliLonchophylla mordax

Macrophyllum macrophyllum

Mimon cozumelae

Phylloderma stenops

Figure 4. Maximum clade credibility tree for the Noctilionoidea showing parsimony-based (left) and likelihood-based (right) ancestral-

state reconstructions: white circle = unfused, partially fused, or variable; black circle = fully fused; black-and-white circle = equivocal

ancestral-state reconstruction (pie charts show the relative likelihood for each character state). The gray rectangle indicates the position

where a reversal is inferred to have occurred. Branch lengths are not to scale, but ages of selected internal nodes are given in millions of

years (Ma).

DiscussionPATTERNS OF SYMPHYSEAL EVOLUTION IN BATSAnalysis of symphyseal evolution in vespertilionoid chiropterans

indicates that reversals from complete ossification do occur and

may be common in some clades. On the other hand, while the

results of our examination of the Noctilionoidea are inconclusive,

it appears that reversals, if they have occurred in this group, are

far less common than they are in vespertilionoids, hinting at an

important difference in symphyseal evolution between these two

superfamilies. It is important to emphasize that we have sampled

only a fraction of living noctilionoids (approximately 18%), and

that further sampling of this group may blur this apparent distinc-

tion. However, it is worth noting that in response to one reviewer’s

comments, we more than doubled the size of our noctilionoid

sample from 15 to 32 species, and of these additional taxa, only

a single one (M. waterhousii) has an unfused symphysis. Thus, it

appears that symphyseal evolution in noctilionoids resembles that

in anthropoid primates to some extent—that is, stasis in symphy-

seal form over millions of years despite a high level of ecological

diversity, including frugivory, insectivory, nectarivory, and car-

nivory (e.g., Norberg and Rayner 1987).

The fact that these two superfamilies present such contrast-

ing patterns suggests that vespertilionoids and noctilionoids may

represent a model system that can be used to understand why

fusion is ubiquitous in anthropoids. In this context, it is no-

table that although many studies have investigated the functional

significance of increased symphyseal ossification, particularly

in primates (Beecher 1977a,b, 1979; Hylander 1979a,b, 1984;

Hylander et al. 1987, 1992, 1998, 2000, 2011; Ravosa 1991,

1996, 1999; Hylander and Johnson 1994; Ravosa and Hylander

1994; Ravosa and Hogue 2004; Vinyard et al. 2005, 2006, 2007;

Scott et al. 2012; for other mammals, see Scapino 1981; Freeman

1995; Hogue and Ravosa 2001; Ravosa and Hogue 2004; Williams

et al. 2008; Davis et al. 2010; Scott et al. 2012), very few attempts

have been made to explain why selection might favor an unfused

symphysis. Researchers who have examined this question have

suggested that a mobile joint may be important for certain types

of occlusion (Scapino 1965, 1981; Crompton and Hiiemae 1970;

Hylander 1979a; Freeman 1995; Scott et al. 2012), but no study

has evaluated differences in chewing performance among taxa that

vary in symphyseal form. The Chiroptera may represent a natural

experiment that can be used to test hypotheses regarding these is-

sues. Importantly, our results provide the first clear demonstration

(to our knowledge) of decreased ossification of the symphyseal

joint in a mammalian clade, indicating that either (1) a mobile

symphyseal joint is selectively advantageous in some contexts or



(2) an ossified symphysis will become unfused via neutral pro-

cesses in the absence of selection to maintain fusion. Establishing

which of these factors accounts for reversal in vespertilionoids,

or if both contribute, is critical.

It is important to recognize that the determinants of symphy-

seal fusion in bats are still poorly understood. Differences in jaw-

muscle activity patterns between Myotis lucifugus (Kallen and

Gans 1972), which has an unfused joint, and Pteropus giganteus

(De Gueldre and De Vree 1988), which has a fused joint, suggest

that variation in symphyseal form may be related to masticatory

stresses along the symphysis (Ravosa and Hogue 2004). However,

complete ossification is observed in all dietary categories repre-

sented in our sample, including frugivores, insectivores, nectari-

vores, carnivores, and sanguivores (based on dietary characteri-

zations presented in Norberg and Rayner 1987; Schondube et al.

2001; Van Cakenberghe et al. 2002). Although the experimental

and comparative studies conducted on primates provide strong

support for the hypothesis that increased symphyseal ossification

in this clade functions to resist elevated joint stresses, which are a

concomitant of processing mechanically challenging foods (e.g.,

Hylander et al. 1992, 2000; Hylander and Johnson 1994), other

factors have been implicated in the case of chiropterans. For ex-

ample, Freeman (1995) linked fusion to the use of the tongue in

food acquisition in nectarivorous bats, and Davis et al. (2010)

argued that complete ossification in the vampire bat Diphylla is

related to the positioning of the incisor teeth in relation to the

symphyseal joint. Thus, if bats are to be used as a model system

for testing hypotheses about the selective advantage of an unfused

symphysis, it is necessary to firmly establish which factors lead

to fusion in this clade.

WHY MIGHT SYMPHYSEAL FUSION BE

CONSTRAINED IN SOME CLADES?

Given the pattern-based approach adopted here, our analysis can-

not identify the evolutionary mechanism responsible for stasis

of symphyseal fusion in the Anthropoidea (and possibly some

noctilionoids) (Wagner 1995). As noted in the introduction, the

invariance of symphyseal form in anthropoids in the face of re-

markable ecological diversity suggests that stabilizing selection

related to environmental factors (i.e., external selection) is not the

primary mechanism driving this phenomenon, thus implicating

the action of some sort of evolutionary constraint. In a brief dis-

cussion of symphyseal fusion in anthropoids, Lockwood (2007)

raised two possibilities. The first is developmental canalization

(e.g., Hallgrımsson et al. 2002; Siegal and Bergman 2002). Ac-

cording to this hypothesis, the developmental program of the

anthropoid symphyseal joint was buffered from the action of ex-

ternal selection pressures very early in the history of this clade.

Such buffering may have occurred because of the adaptive impor-

tance of symphyseal fusion; for example, the symphyseal joint

of the last common ancestor of crown anthropoids may have

been subjected to extended periods of intense diet-related stabi-

lizing selection that eventually resulted in a highly conservative

system.

The observation that fusion occurs very early in ontogeny

in anthropoids—prior to weaning (Schultz 1956, 1969, 1973;

Ravosa 1999)—may be particularly important in this context.

Strepsirrhine primates that exhibit complete ossification (i.e., sub-

fossil lemurs and Eocene adapids) are all “late-fusers” (Ravosa

and Simons 1994; Ravosa 1996, 1999), meaning that fusion is

not achieved until well after weaning has occurred. This differ-

ence in timing may reflect a distinction between anthropoids and

other primates characterized by symphyseal fusion in the degree

to which joint ossification is developmentally buffered. It may

also signal a difference in the adaptive importance of fusion. For

example, the mechanical challenge posed by the diets of some

species may require that the symphysis be fused prior to the time

when an individual adopts adult feeding behaviors (i.e., postwean-

ing; Ravosa 1999), whereas complete ossification (as opposed to

advanced partial fusion) may not be as critical in species in which

fusion occurs relatively late in development. Thus, taxa that re-

quire early-fusing symphyses may be under strong selection for

developmental canalization of this feature. These ideas are dif-

ficult to test, but an initial step in evaluating them would be to

examine the developmental timing of fusion in chiropterans. Of

particular interest is whether bat lineages in which reversion has

occurred are characterized by late-fusing or early-fusing symphy-

ses. A comparison between vespertilionoids, in which reversal

appears to be relatively common, and noctilionoids, in which

reversal appears to be less common (or absent, suggesting the

existence of a potentially anthropoid-like constraint), might be

especially illuminating.

The second possibility suggested by Lockwood (2007) de-

rives from a concept articulated by Wagner and Schwenk (2000)—

the evolutionarily stable configuration (ESC). An ESC is a char-

acter complex that remains stable through the action of internal

selection to maintain functionality of a tightly integrated system,

despite changes in ecology or environmental conditions. From

this perspective, anthropoid symphyseal form is constrained from

varying by the configuration of the other components of its func-

tional system (i.e., the masticatory apparatus). In discussing this

idea, Lockwood (2007) invoked Ravosa et al.’s (2000) argument

that complete ossification of the symphysis in anthropoids is a

functional outcome of changes in skull architecture (related to

increased encephalization) that altered chewing kinematics such

that the balancing-side deep masseter came to play a key role

in effecting transverse jaw movements at the end of the chewing

cycle. Experimental evidence indicates that the horizontal compo-

nent of the force generated by this muscle bends the balancing-side

mandibular corpus laterally, whereas the horizontal component of



the bite force bends the working-side corpus in the opposite direc-

tion, generating a loading regime at the symphysis—referred to as

lateral transverse bending, or wishboning—that an unfused joint

is ill-equipped to resist (Hylander 1984; Hylander et al. 1987,

1998, 2000, 2011; Ravosa 1991, 1999; Hylander and Johnson

1994; Ravosa and Hylander 1994; Ravosa and Hogue 2004; Vin-

yard et al. 2005, 2006, 2007). According to this scenario, then,

the anthropoid symphysis will remain fused as long as the other

elements of its functional system are configured in a way that

leads to wishboning of the mandible during mastication.

The late-firing balancing-side deep masseter (referred to

hereafter as the late deep masseter) has been recorded in all non-

human anthropoid primates examined so far, including macaques,

baboons, owl monkeys, marmosets, and tamarins (Hylander et al.

1987 1998, 2000, 2011; Hylander and Johnson 1994; Vinyard et

al. 2006, 2007). Although this sample represents only a small

fraction of extant anthropoid taxonomic diversity, the fact that

species as distantly related and as ecologically and morphologi-

cally dissimilar as baboons and marmosets possess the late deep

masseter suggests that this muscle-recruitment pattern probably

characterizes most crown anthropoids. The late deep masseter is

also observed in other mammals with fusion or advanced degrees

of partial fusion (Herring and Scapino 1973; Weijs et al. 1989;

Williams et al. 2007; Hylander et al. 2011).

The scenario described above is complicated by two obser-

vations. The first is that humans do not appear to possess a late

deep masseter (Van Eijden et al. 1993). The second is that prelim-

inary data for the New World monkey Cebus apella suggest that

wishboning, if it does occur, is not the dominant loading regime

in the symphysis of this taxon (Vinyard et al. 2011). Persistence

of fusion in the absence of the phenomenon that appears to cause

it is more consistent with the idea that the anthropoid symph-

ysis is developmentally canalized, but these apparent exceptions

do not necessarily refute the argument that a fused symphysis

is an integral component of an anthropoid masticatory ESC. For

example, it may be that the human muscle-recruitment pattern

evolved relatively recently and that natural selection (or drift) has

not had sufficient time to produce an unfused symphysis. It is

also possible that wishboning is not the only loading regime that

requires a fused symphysis (Ravosa and Hogue 2004). According

to Wagner and Schwenk (2000, p. 160), the components of an

ESC are not necessarily invariant (although some may be); rather,

an ESC “comprises a set of phenotypes that vary within certain

functional parameters, rather than a single, fixed form” (empha-

sis added). Thus, perhaps the human and Cebus patterns simply

represent intra-ESC variation. Testing the hypothesis that stasis in

symphyseal fusion in anthropoids is due to membership in an ESC

will require a better understanding of within- and between-clade

variation in patterns of muscle recruitment and mandibular strain

in the Anthropoidea and Strepsirrhini. Similar analyses in other

taxa would further inform our understanding of constraints on the

evolution of the mammalian feeding apparatus.

ConclusionsIn summary, our results are consistent with the idea that the mor-

phology of the mandibular symphyseal joint is evolutionarily con-

strained in some mammalian lineages. Although reversals from

full fusion in speciose clades such as the Anthropoidea and per-

haps the Noctilionoidea have not occurred or are rare, re-evolution

of an unfused joint appears to have been common over the course

of vespertilionoid evolution. We have identified a number of av-

enues of future research that are critical in terms of further testing

the constraint hypothesis and identifying its exact nature. These

include the following: (1) establishing why selection might fa-

vor an unfused symphysis, (2) determining whether the devel-

opmental timing of the onset of fusion influences symphyseal

evolution, and (3) circumscribing the range of biomechanical en-

vironments in which fusion occurs. Comparative analysis of the

two chiropteran superfamilies examined here will undoubtedly

provide greater insight into these issues, particularly the first two.

In vivo studies of muscle-recruitment patterns and mandibular

bone strain during mastication on a greater number of mam-

malian taxa will also be necessary in terms of providing an ap-

propriate functional context in which to evaluate the evolution of

constraint.

ACKNOWLEDGMENTSSpecial thanks to R. Beecher for sharing his data and to N. Cooper, E.Goldberg, V. Lynch, and Wayne Maddison for technical assistance. Wealso thank K. Lewton, G. Wagner, the editors and anonymous reviewers,and the curators and staff at the Field Museum, especially W. Stanley, L.Heaney, and B. Patterson. Financial support for this research was providedto MJR by the NSF (BCS-1029149, BCS-0924592).

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Associate Editor: C. Klingenberg

Supporting InformationThe following supporting information is available for this article:

Appendix S1. Maximum clade credibility tree for Chiroptera in Newick format (with branch lengths in millions of years before

present).

Table S1. GenBank accession numbers.

Supporting Information may be found in the online version of this article.

Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting information supplied by the

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