A timescale for the evolution of lice

A timescale for the evolution of lice Vincent S. Smith with Tom Ford, Kevin Johnson, Paul Johnson, Kazunori Yoshizawa, and Jessica E. Light

Louse phylogeny (eight years on…)
60+ phylogenies! (circa 25 in 2003)
Now cover 90% of louse genera
Mix of molecules & morphology
Beginning to reconcile differences
Very unusual mit. & nuclear genome
New questions emerging via next gen.
One full genome (more coming)
Amblycera Ischnocera Rhynchophthirina Anoplura [ “ Psocoptera” ] 68 spp. (15%) 18 Genera 1427 seq. +29 seq.* 1 spp. (33%) 1 Genus 12 seq. +3 seq.* 509 spp. (17%) 95 Genera 2264 seq. +285 seq.* 134 spp. (10%) 37 Genera 326 seq. +29 seq.* 286 spp. 113 Genera 1218 seq. +478 seq.* GENBANK (June 2011) *Change since Feb. 2010 http: //phylota .net/

Why deep branch louse phylogeny is important?
Permanent obligate parasites
Has ecological replicates
Opportunity to identify ancestral host
Tied to origin of feathers and hair
Model for cospeciation studies at different scales
Need to date the origin of lice

Wappler, Smith & Dalgleish First fossil louse Proc. R. Soc ., 2004. P s o c o p t e r a M e n a c a n t h u s / M e n o p o n - c o m p l e x R i c i n i d a e L a e m o b o t h r i i d a e B o o p i i d a e A u s t r o m e n o p o n - c o m p l e x D e n n y u s - c o m p l e x C o l p o c e p h a l u m - c o m p l e x
Collected Eckfeld maar near Eifel, Germany
Middle Eocene (Middle Lutetian, 44.3±0.4 Ma)
First fossil louse
Completes ordinal representation of fossil insects
Excellent preservation
Phylogenetic affinities with modern feather lice
Parasite of Anseriformes or Charadriiformes
Crown group position
Suggests lice are very old
Points to a long coevolutionary history with birds
Useful molecular calibration point

Not fossil lice! “ Amblyceropsis indica” Kumar (2004) considered a mite by Dalgleish, Palma, Price, & Smith 2006 fused head and thorax (cephalothorax) “ Anopluropsis khatamaensis” Kumar (2004) considered an orbatid mite by Dalgleish, Palma, Price, & Smith 2006

Not fossil lice! Saurodectes vrsanski Rasnitsyn & Zherikhin (1999) “ insect of uncertain ordinal affinities” by Grimaldi and Engel 2005 & Dalgleish, Palma, Price, & Smith 2006 pterosaur louse !

Molecular dating
Build a tree
Character change

Molecular dating
Build a tree
= time

Molecular dating
Build a tree
Test for molecular clock
Now Age of lice

Molecular dating
Build a tree
Rates of evolution vary Now Age of lice

Molecular dating
Build a tree
Apply calibrations

Molecular dating
Build a tree
Apply calibrations
Smooth rates across the tree
R8s with Penalized Likelihood (Sanderson, 2003)
Multidivtime (Thorne et al, 1998)
BEAST (Drummond et al, 2006)
Now Age of lice

Louse phylogeny Amblycera Ischnocera Anoplura Rhynchophthirina
3 Genes (COI, EF1, 18s)
No molecular clock
Eight calibration points
Bayesian Analysis (MrBayes)
- 4 chains, 10 million generations
Recovers classical
louse phlogeny (Grimaldi & Engel 2006) 100 Ma min. Fossil Liposcelid booklouse 19.8 Ma min. Base of the Columbidae (fossil) (Benton 1993) Oldest fossil Diomedeidae- 37 - 53.25 Ma Oldest fossil Procellariform (Benton 1993) 49 Ma min. Oldest Pelicaniform fossil (Mayr 2002) 20 - 25 Ma Old World Monkeys & apes (Reed et al 2004) 5-7 Ma Chimpanzees & humans (Reed et al 2004) 4.75 - 30 Ma Last extant gopher fossil - (Russel 1968) gophers split from relatives 44 Ma min. (Wrappler et al 2004) Fossil Megamenopon louse

Louse phylogeny Fossil Louse (Wappler et al 2004) 44 Myr Fossil louse, Megamenopon

Louse phylogeny Dove-Louse Cospeciation (Benton 1993) 19.8 Myr Base of the Columbidae (fossil)

Louse phylogeny (Benton ed. 1993) 37 - 53 Ma Range for Diomedeidae based on fossils Albatross-Louse Cospeciation Hosts: Albatrosses Parasites: Feather Lice

Louse phylogeny (Reed et al 2004) 5-7 Ma Fossil & Molecular data Chimpanzee-human louse cospeciation

Louse phylogeny (Reed et al 2004) 20-25 Ma Fossil & Molecular data Old World Monkeys - Apes cospeciation

Louse phylogeny Amblycera 79 Ma (57-102 Ma) Ischnocera 98 Ma (74-125 Ma) Anoplura 74 Ma (53-98 Ma) Rhynchophthirina 0 100 Myr KT 105 161 130 Myr (Grimaldi & Engel 2006) 100 Ma min. Fossil Liposcelid booklouse 19.8 Ma min. Base of the Columbidae (fossil) (Benton 1993) Oldest fossil Diomedeidae- 37 - 53.25 Ma Oldest fossil Procellariform (Benton 1993) 49 Ma min. Oldest Pelicaniform fossil (Mayr 2002) 20 - 25 Ma Old World Monkeys & apes (Reed et al 2004) 5-7 Ma Chimpanzees & humans (Reed et al 2004) 4.75 - 30 Ma Last extant gopher fossil - (Russel 1968) gophers split from relatives 44 Ma min. (Wrappler et al 2004) Fossil Megamenopon louse

Louse phylogeny
Lice and hosts must have
a long shared history
Three main clades of lice
parasitizing mammals
Lice are approx. 130 Ma
- 161 - 105 Ma, 95% conf. intervals
Major louse radiation
before the KT boundary Amblycera 79 Ma (57-102 Ma) Ischnocera 98 Ma (74-125 Ma) Anoplura 74 Ma (53-98 Ma) Rhynchophthirina 0 100 Myr KT 105 161 130 Myr

Host implications
Lice radiated on birds first
Mammal lice are young
These groups colonized mammals
What were the first louse hosts? Placental Mammals Marsupials Birds Did lice radiate with feathers? feathers hair

Summary
Just one fossil louse, but..
Many other calibration points
Lice are approx. 130 Ma old
Radiated before dinosaurs when extinct
First radiated on the lineage leading to birds
Either modern birds are older than we think, or…
Perhaps the bird-like Theropod dinosaurs had lice?
Radiated in response to the evolution of feathers?

Press Smith et al 2011. Multiple lineages of lice pass through the K–Pg boundary. Biology Letters doi:10.1098/rsbl.2011.0105

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A timescale for the evolution of lice

by Vincent Smith

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