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)

AmblyceraAmblycera

IschnoceraIschnocera

RhynchophthirinaRhynchophthirina

AnopluraAnoplura

[ “[ “Psocoptera”Psocoptera”]]

68 spp. (15%)18 Genera1427 seq.+29 seq.*

1 spp. (33%)1 Genus12 seq.+3 seq.*

509 spp. (17%)95 Genera2264 seq.+285 seq.*

134 spp. (10%)37 Genera326 seq.+29 seq.*

286 spp.113 Genera1218 seq.+478 seq.*

GENBANK(June 2011)

*Change since Feb. 2010http://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

Psocoptera

Menacanthus /Menopon - complex

Ricinidae

Laemobothriidae

Boopiidae

Austromenopon- complex

Dennyus- complex

Colpocephalum- complex

• 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

Wappler, Smith & Dalgleish

First fossil louse

Proc. R. Soc., 2004.

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

i. Build a tree

Cha

ract

er c

hang

e

Molecular dating

i. Build a tree

= ti

me

Molecular dating

i. Build a tree

ii. Test for molecular clockNow

Age of lice

Molecular dating

i. Build a tree

ii. Test for molecular clock

Rates of evolution vary

Now

Age of lice

Molecular dating

i. Build a tree

ii. Test for molecular clock

iii. Apply calibrations

Molecular dating

i. Build a tree

ii. Test for molecular clock

iii. Apply calibrations

iv. Smooth rates across the tree

- R8s with Penalized Likelihood (Sanderson, 2003)

- Multidivtime (Thorne et al, 1998)

Now

Age of lice

- BEAST (Drummond et al, 2006)

0.1

Louse phylogeny

Amblycera

Ischnocera

Anoplura

Rhynchophthirina

• 3 Genes (COI, EF1, 18s)

• No molecular clock

• Bayesian Analysis (MrBayes)- 4 chains, 10 million generations

• Recovers classical

louse phlogeny

• Eight calibration points

(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

0.1

Louse phylogeny

(Wappler et al 2004)

44 MyrFossil louse, Megamenopon

Fossil Louse

0.1

Louse phylogeny

(Benton 1993)

19.8 MyrBase of the Columbidae (fossil)

Dove-Louse Cospeciation

0.1

Louse phylogeny

(Benton ed. 1993)

37 - 53 MaRange for Diomedeidae based on fossils

Albatross-Louse Cospeciation

Hosts:Albatrosses

Parasites:Feather Lice

0.1

Louse phylogeny

(Reed et al 2004)

5-7 MaFossil & Molecular data

Chimpanzee-human louse cospeciation

0.1

Louse phylogeny

(Reed et al 2004)

20-25 MaFossil & Molecular data

Old World Monkeys - Apes cospeciation

Louse phylogeny

Amblycera79 Ma(57-102 Ma)

Ischnocera98 Ma(74-125 Ma)

Anoplura74 Ma(53-98 Ma)

Rhynchophthirina

0100 Myr

KT105161

130 Myr

0.1

(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

• Lice and hosts must have

a long shared history

Louse phylogeny

• 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

Amblycera79 Ma(57-102 Ma)

Ischnocera98 Ma(74-125 Ma)

Anoplura74 Ma(53-98 Ma)

Rhynchophthirina

0100 Myr

KT105161

130 Myr

Host implications

• Lice radiated on birds first

• Mammal lice are young

• These groups colonized mammals

Placental Mammals

Marsupials

Birds

What were the first louse hosts?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?

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

Questions?