microhabitat specialization in parasitic lice: The evolution of microhabitat specialization in parasitic lice: lineage assortment or character displacement? Vincent S. Smith & Kevin P. Johnson Illinois Natural History Survey University of Illinois Campus Champaign, Illinois USA

…Niche Specialization Head lice Wing lice Body lice

Niche Specialization is Common Opisthocomiformes Passeriformes Galliformes Tinamiformes Charadriiformes Anseriformes Coraciiformes

Patterns of Niche Evolution Body Head Wing B H W CI 1.00 CI 0.33 Niche conserved Niche convergent

? Process of Niche Evolution - consider hosts Niche evolves early Anseriformes A Galliformes G Tinamou T ? Niche evolves early Niche evolves late (niche assorts with host lineages) (niche displaces within host lineages)

Louse Phylogeny Morphology Molecules - 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 Morphology Molecules Topologies Very Different! Principal coordinate analysis of partition metric scores ( subset of these taxa but including more genes) Posterior Prob. > 0.95 Combined Tree 2 islands morph. trees Mol. trees Bootstrap > 0.85 138 characters PAUP* Parsimony, TBR 4 genes (12s, COI, EF1-a, wingless) MrBayes (partitioned by gene) 4 chains, 5 million generations

Niche Evolution Morphology Molecules RI 0.65 CI 0.25 12 steps RI 0.31

Randomization Tests - character fit Morphology Molecules Frequency Niche shuffled across morphological phylogeny (1000 Randomizations, 17-27 steps, RI 0.08-0.469) 50 100 150 200 250 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 RI 0.65 12 steps Actual tree Sig. (P < 0.001) Niche shuffled across molecular phylogeny (1000 Randomizations, 17-22 steps, RI 0.08-0.469) 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 steps Actual tree Not Sig. (P = 0.19) RI 0.31 30 steps Actual tree Sig. (P=0.011) Host shuffled across morphological phylogeny (1000 Randomizations, 29-37 steps, RI 0.00-0.309) 50 100 150 200 250 300 350 29 30 31 32 33 34 35 36 37 Host shuffled across molecular phylogeny (1000 Randomizations, 29-37 steps, RI 0.00-0.409) 50 100 150 200 250 300 350 26 27 28 29 30 31 32 33 34 35 36 37 RI 0.65 12 steps Actual tree Sig. (P < 0.001)

(sister taxa occupying a different niche) Randomization Tests (sister taxa occupying a different niche) Morphological Phylogeny Not significant (P = 1.0) 800 Same Host Order Diff. niche # sister taxa pairs No. of sister taxon pairs from the same host order occupying different ecological niches (1000 Randomized trees) Frequency 700 600 500 Molecular Phylogeny Highly significant (P < 0.001) 400 300 200 100 1 2 3 4 5 6 7 8 9

Niche Evolution - Recap Morphology Molecules Sig.better than random Niche Not significant Host Sig.better than random (just) Sig.better than random Sister taxon niche pairs Not significant Highly significant

? Lineage assortment or character displacement? Morphology Molecules supports lineage assortment Molecules supports character displacement Niche evolves early Niche evolves late (niche assorts with host lineages) (niche displaces within host lineages)

Which hypothesis is best supported? Molecules Niche evolves late (displaces within host lineages) Character displacement Mol. phylogeny well supported Mol. data blind to niche Especially terminal clades There are only a few host niches Mit. + nuclear genes agree We would expect to see strong selection & morphological character convergence

- phylogenetically speaking What use is morphology? - phylogenetically speaking 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

Identifying co-varying characters? Niche Constraint Morphology Repeat until no more characters improve their fit Enforce backbone constraint Which characters fit the constraint tree better than the original? Exclude characters with increased RI Heuristic search 9 cycles, 61 characters excluded We need a better method - any suggestions? Almost half the dataset removed! Remaining characters very noisy

Is character displacement common? Generic phylogeny of sucking lice Genera are sister taxa! Common mammal lice Traditionally considered unrelated Placed in different families Morphologically very different Occupy different host niches

Is character displacement common? Generic phylogeny of sucking lice Human head louse Human pubic louse

Radiation of Anolis lizards on the Greater Antilles Character displacement - a general mechanism producing phenotypic diversity Radiation of Anolis lizards on the Greater Antilles UPGMA Morphology (clusters phenotype) Molecular Phylogeny (phenotype transitions common) Niche / Microhabitat Losos et al. Science 279. 2115-2118

Character displacement - a general mechanism producing phenotypic diversity Fig wasps Weiblen & Bush Mol. Ecol. 11. 1573-1578 Non pollinating Fig wasp parasites Fig Plant hosts Shared host use by wasp sister taxa promotes character displacement

National Science Foundation Acknowledgements National Science Foundation