Coevolution

Session 1fEvolution Meetings – Chico 2003

Ancient Mariners & Recent Stowaways:the coevolution of seabirds & their lice

Division of Environmental and Evolutionary BiologyInstitute of Biomedical and Life Sciences

Graham Kerr BuildingUniversity of Glasgow

Scotland

Vincent S. Smith & Roderic D.M. Page

Parasites… ancient associatesor recent acquisitions?

time

Cospeciation

Extinction

In situ radiation

Serial colonisation

Recent colonisation

Diversification byhost switching

HostParasite

Time isimportant!

The Hosts & Parasites

Feather lice(Insecta: Phthiraptera)

Tubenose seabirds(Aves: Procellariiformes)

Tubenose seabirds are very lousy!

Ischnocera

Charadriiformes

ProcellariiformesN

umbe

r of l

ouse

spe

cies

Procellariif

ormes

Charadriiform

es0

1

2

3

4

5

6Ischnocera

Analysis

ii. Rates smoothing• nonparametric rate smoothing using r8s (Sanderson, 2003)• perform on 100 trees drawn from Bayesian chain

iii. Calibration• assume that cospeciating host/parasites are likely to be the same age• penalised likelihood to estimate the relative age of the other nodes

i. Host/parasite phylogenies• mitochondrial 12s rRNA, COI & Cyt. B• Bayesian analysis (trees sampled every 1000 generations after ‘burnin’)

Albatross-louse cophylogeny

0.01

Macronectes giganteus

Diomedea epomophora

Diomedea exulans

Diomedea gibsoni

Diomedea antipodensis

Phoebastria nigripes

Phoebastria irrorata

Thalassarche chrysostoma

Thalassarche melanophris

Thalassarche cauta

Thalassarche bulleri

Phoebetria palpebrata

0.1

Paraclisis obscura

Paraclisis hyalina NZ AP16

Paraclisis hyalina FD03

Paraclisis hyal ina GLA901

Paraclisis hyal ina GLA896

Paraclisis confidens

Paraclisis miriceps

Paraclisis d iomedeae FD07

Paraclisis d iomedeae FD10

Paraclisis diomedeae GLA529

Paraclisis diomedeae NZ AP21

Paraclisis d iomedeae FD05

Hosts:Albatrosses

Parasites:Feather Lice

Page et al (in press)Mol. Phyl. Evol.

Analysis

v. Tree mapping• identify comparable nodes in the host & parasite tree• compare ages of nodes

ii. Rates smoothing• nonparametric rate smoothing using r8s (Sanderson, 2003)• perform on 100 trees drawn from Bayesian chain

iii. Calibration• assume that cospeciating host/parasites are likely to be the same age• penalised likelihood to estimate the relative age of the other nodes

iv. Sensitivity analyses• rate smoothing is sensitive to choice of smoothing parameter• we varied the log of the parameter for each of the 100 bird/louse trees

i. Host/parasite phylogenies• mitochondrial 12s rRNA, COI & Cyt. B• Bayesian analysis (trees sampled every 1000 generations after ‘burnin’)

Procellariiform-louse tanglegram

0.1 substitu tions per s ite

Thalassarche bulleri

Phoebastria nigripes

Diomedea exulans

1.00

1.00

1.00

Pelagodroma marina

0.60

Macronectes giganteus

Daption capense

1.00

Puffinus gravis

Puffinus griseus

1.00

Puffinus pacificus

1.00

Puffinus huttoni

0.96

Calonectris diomedea

1.00

Procellaria westlandica

1.00

Pelecanoides georgicus

Lugensa brevirostris

Pachypt ila vittata

Pachyptila turtur

1.000.60

0.94

0.33

Pterodroma inexpectata

Pterodroma cooki

1.00

0.44

1.00

0.95

Paraclisis diomedeae

Paraclisis conf idens

Paraclisis hyalina

Paraclisis hyalina

1.00

Paraclisis obscura1.00

1.00

0.99

Perineus concinnoides

Harrisoniella hopkinsi

1.00

0.77

Pelmatocendra enderleini

0.35

Halipeurus pelagicus

Halipeurus diversus

Halipeurus gravis

Halipeurus spadix0.82

Halipeurus abnormis

Halipeurus consimilis

1.00

0.99

0.73

0.98

0.70

Naubates harrisoni

Naubates fuliginosus 1.00

1.00

Pseudonirmus gurlt i

1.00

Naubates pterodromi 0.69

0.30

0.18

Bedfordiella unica

1.00

0.1 s ubs ti tu tions per s ite

Diomedea epomophora

Halipeurus turtur

Naubates prioni

Naubates prioni

0.67

Bayesian inference(12s rRNA, COI & Cyt. B)

Are procellariformlice as old as their hosts?

• Age estimates relatively constant across arange of smoothing parameters

• Radiation of procellariform lice is slightlymore recent than that of their hosts

log 10 smoothing

3

2.5

2

1.5

1

0.5

0

0 0.5 1 1.5 2.52 3

Procellariiformes

rela

tive

age

Procellariform birds 2-2.5 timesolder than albatrosses

0

3

2.5

2

1.5

1

0.5

0 0.5 1 1.5 2.52 3

Feather lice

log 10 smoothing

rela

tive

age

Feather lice 1.75-2.25 timesolder than albatross lice

Bird-Louse Ages

T halas sarche buller i

P hoebas tria n igripes

Diomedea ex ulans

Diomedea epomophor a

Pelagodroma mar ina

Macr onectes giganteus

Daption capense

Pelecanoides georgicus

Lugensa brevir os tris

Pachyptila v itta ta

Pachyptila turtur

Pterodr oma inex pectata

Pterodr oma cook i

Py gosc el is adeliae

Eudyptula m inor

Gavia arctica

Gavia immer

Puffinus griseus

Puffinus grav is

Puffinus hutton i

Calonectris d iomedea

Procel laria westlandica

Thalass arche bulleri

P hoebastria n igripes

Diomedea exulans

Diomedea epomophora

Pelagodroma marina

Macr onectes giganteus

Daption capense

Pelecanoides geor gicus

Lugensa brevir os tr is

Pachyptila vitta ta

Pachyptila turtur

Pterodroma inex pec tata

Pterodroma cook i

Py gosc el is adeliae

Eudyptu la m inor

Gavia arctica

Gavia immer

Parac lisis d iomedeae

Paraclisis confidens

Paraclisis hyalina

Par ac lisis hy al ina

Paracl isis obs cura

Naubates harr isoni

Naubates fu liginos us

Puffinus gr iseus

Puffinus gr av is

Puffinus hutton i

Calonectris d iomedea

Procellaria wes tlandica

Halipeurus pelagicus

Hal ipeurus diversus

Hal ipeurus gravis

Halipeurus spadix

Halipeurus abnorm is

Hal ipeur us c onsimi l is

Hal ipeurus turturi

Naubates prioni

Naubates prion i

Naubates pterodromi

Perineus concinnoides

Harr isonie l la hopkins i

relative age relative age123 0 0 1 2 0 1 2

• How do we accountfor this?

?

Relative Age of Host-Parasite Clades

0

0.5

1

1.5

2

2.5

0 0.5 1 1.5 2 2.5

Host Age

Lous

e A

gePetrels & Halipeurus

Procellariformes &Philoceanus-complex

• Lice ¾ of the ageof their hosts!

• i.e lice are slightlyyounger than wemight expect if theyare “cospeciating”

Conclusions

i. Is this discrepancy real?• Are the assumptions behind the calibration point correct

Calibration Correction?Hosts:Albatrosses

Parasites:Feather Lice

-0.4

-0.2

0

0.2

0.4

0.6

0.8

1

1.2

1.4

0.02 0.04 0.06 0.08 0.1 0.12

Host divergence

Lous

e di

verg

ence Delayed

cospeciation

i.e. Paraclisisspeciating slightlyafter their hosts

Conclusions

iii. Do we need to redefine “cospeciation”• Is the expectation of temporal congruence always correct in

cospeciating lineages?

i. Is this discrepancy real?• Are the assumptions behind the calibration point correct

ii. If it is real, what does it mean?• Gene flow briefly persists between lice after speciation of the host?• Failure of lice to speciate (Johnson et al, 2003)• Aren’t we really dating gene coalescent times anyway?

(Rannala & Michalakis, 2002)

Acknowledgements

• Martyn Kennedy & Rob Cruickshank

• Wellcome Trust