Did dinosaurs have lice?

Vince Smith, Tom Ford, Kevin Johnson*, Paul Johnson & Rod Page

University of Glasgow, Glasgow, UK

*Illinois Natural History Survey, USA

Fossil 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, Proc.R.Soc., 2004.

Approaches To Dating

i. Test for molecular clock

ii. Establish calibration points- Crown group fossils

- R8s (Sanderson, 2003)

iii. Apply rate smoothing

- Penalized likelihood- Cross validation100

75

50

25

0

100

75

50

25

0

iv. Multiple approaches!- Bottom up- Top down - cospeciation dates

30

20

10

0

v. Compare ages30

20

10

0

100

75

50

25

0

Bot

tom

Up

Top D

own

35 ma

30 ma

i. Test for molecular clock

Phthiraptera

Phthiraptera

18s rRNA COI (1st & 2nd pos.)

ML (GTR+I+G)

ML (TVM+I+G)

0.1 0.1

CrustaceaDictyoptera

Hemiptera

Psocoptera

Lepidoptera

Diptera

CrustaceaOdonata

DictyopteraPlecoptera

Hemiptera

Psocoptera

ColeopteraRaphidiodea

MegalopteraNeuroptera

Hymenoptera

TrichopteraLepidoptera

SiphonapteraMecoptera

Diptera / Strepsiptera

Thysanoptera

EF1- Wingless

ML (GTR+I+G)

ML (GTR+I+G)

0.1 0.1

Phthiraptera

Phthiraptera

Trichoptera

Lepidoptera

SiphonapteraMecoptera

Coleoptera

Hymenoptera

Diptera

Hemiptera

Thysanoptera

Odonata

Hymenoptera

Diptera

Lepidoptera

Coleoptera

Thysanoptera

Hemiptera

Crustacea

0.1 0.1 0.1 0.1

18s rRNA COI EF1- Wingless

Insect Phylogeny (unsmoothed)

Ages Fixed Age Constraints

~185 ma~260 ma ~250 ma~295 ma(280-300 ma) (235-300 ma) (200-250 ma) (185-240 ma)

18s rRNA COI EF1- Wingless

0100200300

Hym

eno

ptera

Dip

teraL

epid

op

teraC

oleo

ptera

Th

ysano

ptera

LIC

EH

emip

tera

Hem

iptera

Dip

teraL

epid

op

tera

0100200300400500

LIC

E

0100200300400

Lep

ido

p.

Cad

dis

Fleas

Meco

p.

Flies

Hym

eno

p.

Co

leop

.L

ICE

Bu

gs

Th

rips

Od

on

ata

0100200300400

Strep

sip.

Flies

Fleas/M

ecop

.

Tric./L

ep.

Hym

eno

p.

Neu

rop

.B

eetlesL

ICE

Bu

gs

Bark L

ice

Insect Phylogeny (rate smoothed)

Cospeciation Events

Constraints

Min. Age 44 ma

Louse Fossil

Combined ML

0.1

(18s, COI, EF1-)

Dove-Louse Cospeciation

Age Fixed 19.8 ma

Rhea/Ostrich-Louse Cospeciation

Age Fixed 60 ma

Primate-Louse Cospeciation

Age Fixed 4.5 ma

Am

blyce

raIsch

no

cera

An

op

lura

Rhyn.

Louse Phylogeny (unsmoothed)

Ricinus spLaemobothrion atrumAustromenopon elliottiTrinoton querquedulaeHolomenopon spDennyus hirundinisMachaerilaemus spColimenopon urocoliusDocophoroides brevisFulicoffula longipilaBovicola spFelicola subrostratusNeotrichodectes spGeomydoecus spPectinopygus sulaePectinopygus brevicornisPectinopygus punctatusPectinopygus variusAnatoecus icterodesTrichophilopterus babakotophilusColumbicola columbaeColumbicola passerinaeStruthioliperus nanduStruthiolipeurus struthionisCraspedorrhynchus spDegeeriella fulvaAustrophilopterus subsimilusColilipeurus coliusCampanulotes comparGoniodes spNaubates spPerineus nigrolimbatusHaematomyzus elephantsPediculus humanus var capitisPediculus schaeffiEchinophthirius horridus bPolyplax spinulosaHaematopinus tuberculatusHaematopinus suisHaematopinus pacochoeriHoplopleura trispinosaHoplopleura spPterophthirus imitansLinognathoides marmotaeLinognathoides marmotae bNeohaematopinus sciuriNeohaematopinus sciuri b

0100200

Louse Phylogeny (rate smoothed)

Combined ML(18s, COI, EF1-)

Am

blyce

raIsch

no

cera

An

op

lura

Rhyn.

~190 ma(150-225 ma)

KT

Result very sensitive to smoothing

parameter used

Host Implications

Paleocene

Cretaceous

Late Cretaceous

Early Cretaceous

Late Jurassic

157ma ±

146ma ±

97ma ±

65ma ±

Modern Birds

‘Ratites’ and

tinamousNeognathae

Neornithes

Archaeopteryx

Paleognathae

Tertiary ‘big bang’ model for modern bird evolution sensu Feduccia, 1995

Figure adapted from Feduccia,

1995

010

020

0

‘Big bang’ followed by a ‘big switch’?

Modern birds much older - Gondwanic origin?

Revised classic model sensu Cracraft, 2001

KT

Modern Birds

Host Implications

Figure adapted from ???,

Science, ????

2-300ma ?

Summary

• Lice are old (150-300ma)

• Major radiation of lice before the KT (65ma)

• Modern birds & lice have a very long coevolutionary history

• Origin of lice associated with origin of feathers?

• Recent threopod dinosaurs probably had lice?

• Molecular clocks run fast at times of rapid radiation?

Caveats

Acknowledgements

• Wellcome TrustQuickTime™ and aTIFF (LZW) decompressorare needed to see this picture.