Host-Parasite Cospeciation
Mar 28, 2015
Host-Parasite Cospeciation
Key Questions
• Is the parasite an heirloom or a souvenier?
• Is the association ancient or recent?
• What processes are involved?
• Is there coevolution?
• Is there correlated evolution?
Coevolution: coadaptation and cospeciation
• Coadaptation = reciprocal adaptation
• Cospeciation = joint speciation of host and parasite
Farenholz’s Rule
• Farenholz’s rule - parasite phylogeny mirrors host phylogeny
• Implies we can use parasite phylogeny to infer host phylogeny
Modern Cospeciation Studies
• Construct host and parasite phylogenies independently.
• Test for cospeciation (don’t assume it).
• Use molecular phylogenies so we can compare rates of evolution.
Host Parasiteincongruence
congruence(cospeciation)
(not cospeciation, e.g. host switching)
Incongruence signals processes other than cospeciation
independent speciationhost switchcospeciation
"missing the boat"extinction
host
parasite
(a) (b)
(e)(d)
(c)
failure to speciate
(f)
Testing hypotheses of cospeciation
• Would we get host and parasite phylogenies that are this similar due to chance alone?
• Can test using random trees: generate many (>100) random parasite trees and see how similar they are to the host tree.
Same topologies, speciation times, and rates of evolution
Same topologies and times of speciation
Same tree topologies(a)
(b)
(c)
Lice as a “model system”
• Methods for comparing host and parasite phylogenies
• Comparative molecular evolution
• Factors involved in cospeciation
• Factors involved in host specificity
GenusFamilySuborder
Anoplura532
Ischnocera3,060
1,344Amblycera
birdmammal
Kim, 1988
Paterson et al,2000
Smith, 2000
Smith, 2000
Barker, 1991
Clayton et al, 1996
Page et al, 1995Hafner et al, 1994
Lyal, 1985a
Rhyncophthirina2
Clay, 1969
Host:
Why lice are nice...
• Obligatory, permanent parasites
• Single host during life cycle
• Ectoparasites (easy to manipulate)
• High degree of cospeciation
Why lice are lousy...
• Single origin of parasitism
• No endoparasitic lice
• Single host during life cycle
• Not (very) virulent
• c.f. mites
Gophers and LiceO. hispidus
T. bottae
T. talpoides
G. personatus
G. breviceps
G. bursarius (a)
G. bursarius (b)
C. merriami
P. bulleri
O. cavator
O. cherriei
O. underwoodi
C. castanops
O. heterodus
Z. trichopus
G. chapini
G. setzeri
G. thomomyus
G. perotensis
T. minor
T. barbarae
G. trichopi
G. nadleri
G. expansus
G. geomydis
G. oklahomensis
G. ewingi
G. texanus
G. actuosi
G. panamensis
G. cherriei
G. costaricensis
Swiftlets and Dennyus liceChaetura pelagica
Chaetura vauxi
C. esculenta nitens
C. esculenta bagobo
C. esculenta marginata
C. esculenta cyanoptila 1
C. esculenta cyanoptila 2
C. linchi
A. elaphrus
A. francicus
A. spodiopygius assimilis 1
A. mearnsi
A. vanikorensis palawanensis
A. fuciphagus vestitus
A. salanganus natunae
A. spodiopygius assimilis 2
A. s. spodiopygius
A. maximus lowi
A. brevirostris vulcanorum
A. terraereginae
Cypsiurus balasiensis
Cypsiurus parvus
D. dubius
D. vauxi
Dennyus sp. 1
D. distinctus ssp.
D. distinctus timjonesi
D. d. distinctusD. somadikartai 1
D. somadikartai 2
D. carljonesi fosteri
D. carljonesi forresteri
D. hahnae
D. c. carljonesi
D. singhi
D. kristinae
D. wraggi
D. simberloffi
Dennyus sp. 2D. wellsi
D. thompsoni
D. collinsi
D. adamsae
D. cypsiurus 1
D. cypsiurus 2
Song birds and Brueelia liceAratinga astecNyctibius jamaicensisFormicarius moniligerThamnophilus doliatusPloceus velatusCacicus haemorrhousCarpodacus mexicanusPycnonotus nigricansHypsipetes philippenisParisoma subcaeruleum
Parus nigerParus elegansSitta frontalisFicedula hyperythraRhipidura nigrocinnamomeaCoracina striata
Cyanocorax morioTrogon massenaTrogon melanocephalusMomotus momotaMelanerpes candidusAndigena nigrirostrisAulacorhynchus prasinusMegalaima monticolaMegalaim mystacophanos
Nyctibicola longirostris
Paragoniocotes sp.
Formicaricola analoides
Formicaphagus sp.
Brueelia sp. 7
Brueelia sp. 6
Brueelia sp. 8
Brueelia sp. 11
Brueelia sp. 9
Brueelia sp. 10
Brueelia sp. 12
Brueelia sp. 5
Brueelia moriona
Brueelia sp. 2
Brueelia sp. 1
Brueelia sp. 3
Brueelia laticeps
Brueelia marginella
Brueelia sp. 4
Correlated evolution
• Relative rates of molecular evolution
• Host and louse body size
• Host and parasite speciation rates
Relative rates of molecular evolution
• Molecular data is comparable between hosts and parasites (unlike morphological data)
• Can use homologous genes to compare rate of evolution (e.g., cytochrome oxidase I in birds and lice)
• Louse mitochondrial genes evolve 2-3 times more rapidly than bird and mammal genes
220
240
260
280
300
320
340
3.00 3.50 4.00 4.50 5.00 5.50 6.00 6.50
Lou
se m
etat
hora
cic
wid
th (
µm
)
ln (Host body mass in grams)
Big birds have big lice
Head groove width correlates with hair width
40 50 60 70 8030
40
50
60
70
80
Gro
ov
e D
iam
ete
r o
f C
he
win
g L
ou
se
(µm
)
Hair Diameter of Pocket Gopher (µm)
host clade
first parasite clade
second parasite clade
Time
2T
1T
Replicate lineages
• Multiple parasites on the same host• Can test hypotheses concerning patterns and
processes
Phoebetria palpebrata
Diomedea chrysostoma
Diomedea bulleri
Diomedea epomophora
Diomedea exulans
Diomedea irrorata
Diomedea nigripes
Diomedea immutabilis0.1
79 Paraclisis diomedeae
78 Paraclisis diomedeae
77 Paraclisis diomedeae
81 Paraclisis hyalina
82 Paraclisis hyalina
80 Paraclisis giganticola
83 Paraclisis miriceps
76 Paraclisis confidens
Diomedea bulleri
Diomedea exulans
Diomedea epomophora
Diomedea immutabilis
Diomedea irrorata0.1
291 Docophoroides harrisoni
290 Docophoroides brevis
289 Docophoroides brevis
293 Docophoroides niethammeri
292 Docophoroides levequei
Distribution of two louse genera
How do multispecies How do multispecies assemblages arise?assemblages arise?
Host species A Host species B
“head” lice
“wing” lice
GenusFamilySuborder
Anoplura532
Ischnocera3,060
1,344Amblycera
birdmammal
Kim, 1988
Paterson et al,2000
Smith, 2000
Smith, 2000
Barker, 1991
Clayton et al, 1996
Page et al, 1995Hafner et al, 1994
Lyal, 1985a
Rhyncophthirina2
Clay, 1969
Host:
How old are lice w.r.t. How old are lice w.r.t. their hosts?their hosts?
present day
time
lice younger lice same age lice older
radiation of modern birds radiation of
bird lice
Microraptor gui, an early Cretaceous feathered dinosaur
Fossil bird louse from Eocene (44 Mya)
Summary
• Host-parasite cospeciation is an instance of a more general problem (“historical associations”).
• We can use phylogenies for host and parasite to test hypotheses of cospeciation.
• Lice are an excellent group for cospeciation studies.