Host defense reinforces host–parasite cospeciation

Cospeciation occurs when interacting groups, such as hosts and parasites, speciate in tandem, generating congruent phylogenies. Cospeciation can be a neutral process in which parasites speciate merely because they are isolated on diverging host islands. Adaptive evolution may also play a role, but this has seldom been tested. We explored the adaptive basis of cospeciation by using a model system consisting of feather lice (Columbicola) and their pigeon and dove hosts (Columbiformes). We reconstructed phylogenies for both groups by using nuclear and mitochondrial DNA sequences. Both phylogenies were well resolved and well supported. Comparing these phylogenies revealed significant cospeciation and correlated evolution of host and parasite body size. The match in body size suggested that adaptive constraints limit the range of hosts lice can use. We tested this hypothesis by transferring lice among hosts of different sizes to simulate host switches. The results of these experiments showed that lice cannot establish viable populations on novel hosts that differ in size from the native host. To determine why size matters, we measured three components of louse fitness: attachment, feeding, and escape from host defense (preening). Lice could remain attached to, and feed on, hosts varying in size by an order of magnitude. However, they could not escape from preening on novel hosts that differed in size from the native host. Overall, our results suggest that host defense reinforces cospeciation in birds and feather lice by preventing lice from switching between hosts of different sizes.

[1]  D. Tompkins,et al.  Ectoparasite virulence is linked to mode of transmission , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  P. Ruben,et al.  References and Notes Materials and Methods Text Figs. S1 and S2 Table S1 References Mechanisms of Adaptation in a Predator-prey Arms Race: Ttx-resistant Sodium Channels , 2022 .

[3]  R. Page,et al.  Comparative body size relationships in pocket gophers and their chewing lice. , 2000 .

[4]  W. Kirk The size relationship between insects and their hosts , 1991 .

[5]  B. C. Nelson,et al.  The distribution of Mallophaga on the domestic pigeon (Columba livia). , 1971, International journal for parasitology.

[6]  F. Hoffmann,et al.  Tangled Trees: Phylogeny, Cospeciation, and Coevolution , 2004 .

[7]  D. Tompkins,et al.  Reciprocal Natural Selection on Host‐Parasite Phenotypes , 1999, The American Naturalist.

[8]  Margaret T. Martin LIFE HISTORY AND HABITS OF THE PIGEON LOUSE (COLUMBICOLA COLUMBAE [LINNAEUS[) , 1934, The Canadian Entomologist.

[9]  R. Poulin Evolutionary Ecology of Parasites , 1997 .

[10]  D. Clayton,et al.  CRITICAL EVALUATION OF FIVE METHODS FOR QUANTIFYING CHEWING LICE (INSECTA: PHTHIRAPTERA) , 2001, The Journal of parasitology.

[11]  S. Morand,et al.  Specificity and host predictability: a comparative analysis among monogenean parasites of fish , 1999 .

[12]  Carol J. Bult,et al.  Constructing a Significance Test for Incongruence , 1995 .

[13]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[14]  C. M. Lessells,et al.  Unrepeatable repeatabilities: a common mistake , 1987 .

[15]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[16]  D. Clayton,et al.  Low humidity reduces ectoparasite pressure: implications for host life history evolution , 2002 .

[17]  J. Murphy,et al.  Herbivory: Caterpillar saliva beats plant defences , 2002, Nature.

[18]  Read,et al.  What makes a specialist special? , 1999, Trends in ecology & evolution.

[19]  K. Crandall,et al.  Phylogeny Estimation and Hypothesis Testing Using Maximum Likelihood , 1997 .

[20]  B. Williams,et al.  The population genetics of host specificity: genetic differentiation in dove lice (Insecta: Phthiraptera) , 2002, Molecular ecology.

[21]  J. Thompson,et al.  The Coevolutionary Process , 1994 .

[22]  D. Clayton,et al.  Nuclear and mitochondrial genes contain similar phylogenetic signal for pigeons and doves (Aves: Columbiformes). , 2000, Molecular phylogenetics and evolution.

[23]  B. Walther,et al.  Influence of host ecology and morphology on the diversity of Neotropical bird lice , 2001 .

[24]  R. Page,et al.  When do parasites fail to speciate in response to host speciation? , 2003, Systematic biology.

[25]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[26]  J. X. Becerra Insects on plants: macroevolutionary chemical trends in host use. , 1997, Science.

[27]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[28]  C. Kennedy Attachment may be a basis for specialization in oak aphids , 1986 .

[29]  A. Peterson,et al.  INFLUENCE OF BILL SHAPE ON ECTOPARASITE LOAD IN WESTERN SCRUB-JAYS , 2002 .

[30]  Roderic D. M. Page,et al.  Temporal Congruence and Cladistic Analysis of Biogeography and Cospeciation , 1990 .

[31]  D. Clayton,et al.  Impact of feather molt on ectoparasites: looks can be deceiving , 2002, Oecologia.

[32]  D. Brooks,et al.  Evolutionary biology of parasites. , 1981, Monographs in population biology.

[33]  Olaf Ellers,et al.  Scaling in biology , 2001, Complex..

[34]  D. Clayton,et al.  Taxonomy of New World Columbicola (Phthiraptera: Philopteridae) from the Columbiformes (Aves), with descriptions of five new species. , 1999 .

[35]  Daniel M. Tompkins,et al.  Host resources govern the specificity of swiftlet lice: size matters , 1999 .

[36]  D. Clayton,et al.  The chewing lice: world checklist and biological overview. , 2003 .

[37]  R. Ricklefs,et al.  Host plants influence parasitism of forest caterpillars , 2002, Nature.