microhabitat specialization in parasitic lice:

lineage assortment or character displacement?

Illinois Natural History SurveyUniversity of Illinois Campus

Champaign, IllinoisUSA

Vincent S. Smith & Kevin P. Johnson

The evolution of

…Niche Specialization

Body lice

Head lice

Wing lice

Niche Specialization is Common

Opisthocomiformes Passeriformes

GalliformesTinamiformes

Charadriiformes

Anseriformes

Coraciiformes

Patterns of Niche Evolution

Niche conserved Niche convergent

Wing WWWHead HHHBody BBB

CI 1.00 CI 0.33

Process of Niche Evolution - consider hosts

Niche evolves early

(niche assorts with host lineages)

Niche evolves late

(niche displaces within host lineages)

?

GalliformesG G G AnseriformesA A A TinamouT T T

Louse Phylogeny

MoleculesMorphology

- 41 in-group taxa (~ 1/3rd ischnoceran genera)

- mammal louse (trichodectid) outgroup

- in-group span basal ischnoceran diversity

- representatives from 18 bird orders

- all but 4 bird orders host lice from 2 or more niches

- include 8 ‘body’, 12 ‘head’, 10 ‘wing’ & 11 ‘generalist’ genera

- focus on avian Ischnocera (Philopteridae)

Louse Phylogeny

• 4 genes (12s, COI, EF1-a, wingless)

• MrBayes (partitioned by gene)

• 4 chains, 5 million generations

Molecules

Posterior Prob. > 0.95

Morphology

• 138 characters

• PAUP*

• Parsimony, TBR

Bootstrap > 0.85

Topologies Very Different!

Principal coordinate analysis of partition metric scores

( subset of these taxa but including more genes)

Combined Tree

Mol. trees2 islands

morph. trees

Niche EvolutionMorphology Molecules

RI 0.31CI 0.1421 steps

RI 0.65CI 0.2512 steps

Randomization Tests - character fitMolecules

RI 0.65

12 stepsActual tree

Sig. (P < 0.001)

Niche shuffled across molecular phylogeny(1000 Randomizations, 17-22 steps, RI 0.08-0.469)

0

50

100

150

200

250

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

RI 0.31

21 stepsActual tree

Not Sig. (P = 0.19)

Host shuffled across molecular phylogeny(1000 Randomizations, 29-37 steps, RI 0.00-0.409)

0

50

100

150

200

250

300

350

26 27 28 29 30 31 32 33 34 35 36 37

RI 0.65

12 stepsActual tree

Sig. (P < 0.001)

Morphology

Fre

qu

en

cy

Niche shuffled across morphological phylogeny(1000 Randomizations, 17-27 steps, RI 0.08-0.469)

0

50

100

150

200

250

12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

RI 0.31

30 stepsActual tree

Sig. (P=0.011)

Host shuffled across morphological phylogeny(1000 Randomizations, 29-37 steps, RI 0.00-0.309)

0

50

100

150

200

250

300

350

29 30 31 32 33 34 35 36 37

Randomization Tests

0

100

200

300

400

500

600

700

800

0 1 2 3 4 5 6 7 8 9

(sister taxa occupying a different niche)

No. of sister taxon pairs from the same host order occupying different ecological niches

(1000 Randomized trees)

Fre

qu

en

cy

Molecular Phylogeny

Highly significant (P < 0.001)

Morphological Phylogeny

Not significant (P = 1.0)

Same Host Order

Diff. niche

# sister taxa pairs

Niche Evolution - RecapMorphology Molecules

Sig.better than random Niche Not significant

Host Sig.better than random (just) Sig.better than random

Sister taxonniche pairs

Not significant Highly significant

Niche evolves early

(niche assorts with host lineages)

Niche evolves late

(niche displaces within host lineages)

?Morphology supports lineage

assortment

Moleculessupports characterdisplacement

Lineage assortment or character displacement?

Which hypothesis is best supported?

Molecules

Niche evolves late(displaces within host lineages)

Character displacement

• Mol. phylogeny well supported

• Especially terminal clades

• Mit. + nuclear genes agree

• Mol. data blind to niche

• There are only a few host niches• We would expect to see strong selection & morphological

character convergence

What use is morphology?

Can we identify morphological characters that co-vary with niche?

If so, what are they, and can we extract them to build the ‘correct’ louse phylogeny

i.e. one that is topologically more similar to the molecular tree

- phylogenetically speaking

Identifying co-varying characters?MorphologyNiche Constraint

Enforce backbone constraint

Which characters fit the constraint tree

better than the original?

Exclude characters withincreased RI

Heuristic search

Repeat until no morecharacters improve their fit

• 9 cycles, 61 characters excluded

• Almost half the dataset removed!

• Remaining characters very noisy

• We need a better method - any suggestions?

Is character displacement common?

• Common mammal lice

• Traditionally considered unrelated

• Morphologically very different

• Occupy different host niches

• Placed in different families

Haematomyzus elephantisHaematomyzus hopkinsiHaematomyzus porciAntarctophthirus callorhiniAntarctophthirus microchirLepidophthirus macrorhiniEchinophthirius horridusLatagophthirus rauschiProechinophthirus fluctusProechinophthirus zumptiMicrothoracius cameliNeolinognathus elephantuliLinognathus aepycerusLinognathus africanusLinognathus setosusProlinognathus aethiopicusProlinognathus ferrisiSolenopotes muntiacusRatemia squamulataAtopophthirus emersoniMicrophthirus uncinatusEnderleinellus osborniWerneckia nigeriensisPhthirunculus sumatranusAncistroplax crociduraeHoplopleura acanthopusHoplopleura irritansHoplopleura pacificaPterophthirus audaxPterophthirus splendidaParadoxophthirus emarginataSchizophthirus graphiuriSchizophthirus pleurophaeusTyphlomyophthirus bifoliatusHaematopinoides squamosusLemurphthirus galagusLemurphthirus stigmosusSathrax durusNeohaematopinus callosciuriNeohaematopinus inornatusPolyplax abyssinicaPolyplax spinulosaAbrocomaphthirus chilensisCtenophthirus cercomydisJohnsonpthirus chlorotalpaeJohnsonpthirus heliosciuriLinognathoides laeviusculusProenderleinellus calvaDocophthirus acinetusLagidiophthirus parvusEulinognathus denticulatusFahrenholzia ferrisiFahrenholzia pinnataHaemodipsus leporisHaemodipsus lyriocephalusGaleophthirus caviaePhthirpediculus brygooiScipio aulacodiScipio tripedatusHamophthirius galeopitheciPecaroecus javaliiPedicinus ferrisiPedicinus patasPediculus humanusPediculus humanus var. americanusPediculus mjobergiPediculus schaeffiPthirus gorillaePthirus pubisHaematopinus asiniHaematopinus suisHybophthirus notophallus

Generic phylogeny of sucking lice

• Genera are sister taxa!

Is character displacement common?

Haematomyzus elephantisHaematomyzus hopkinsiHaematomyzus porciAntarctophthirus callorhiniAntarctophthirus microchirLepidophthirus macrorhiniEchinophthirius horridusLatagophthirus rauschiProechinophthirus fluctusProechinophthirus zumptiMicrothoracius cameliNeolinognathus elephantuliLinognathus aepycerusLinognathus africanusLinognathus setosusProlinognathus aethiopicusProlinognathus ferrisiSolenopotes muntiacusRatemia squamulataAtopophthirus emersoniMicrophthirus uncinatusEnderleinellus osborniWerneckia nigeriensisPhthirunculus sumatranusAncistroplax crociduraeHoplopleura acanthopusHoplopleura irritansHoplopleura pacificaPterophthirus audaxPterophthirus splendidaParadoxophthirus emarginataSchizophthirus graphiuriSchizophthirus pleurophaeusTyphlomyophthirus bifoliatusHaematopinoides squamosusLemurphthirus galagusLemurphthirus stigmosusSathrax durusNeohaematopinus callosciuriNeohaematopinus inornatusPolyplax abyssinicaPolyplax spinulosaAbrocomaphthirus chilensisCtenophthirus cercomydisJohnsonpthirus chlorotalpaeJohnsonpthirus heliosciuriLinognathoides laeviusculusProenderleinellus calvaDocophthirus acinetusLagidiophthirus parvusEulinognathus denticulatusFahrenholzia ferrisiFahrenholzia pinnataHaemodipsus leporisHaemodipsus lyriocephalusGaleophthirus caviaePhthirpediculus brygooiScipio aulacodiScipio tripedatusHamophthirius galeopitheciPecaroecus javaliiPedicinus ferrisiPedicinus patasPediculus humanusPediculus humanus var. americanusPediculus mjobergiPediculus schaeffiPthirus gorillaePthirus pubisHaematopinus asiniHaematopinus suisHybophthirus notophallus

Generic phylogeny of sucking lice

Human head louse Human pubic louse

Character displacement - a general mechanism producing phenotypic diversity

Radiation of Anolis lizards on the Greater Antilles

UPGMA Morphology(clusters phenotype)

Molecular Phylogeny(phenotype transitionscommon)

Niche / Microhabitat

Losos et al. Science 279. 2115-2118

Character displacement - a general mechanism producing phenotypic diversity

Fig waspsWeiblen & Bush Mol. Ecol. 11. 1573-1578

Non pollinatingFig wasp parasites

FigPlant hosts

Shared host use by wasp sister taxa promotes

character displacement

Acknowledgements

National Science Foundation