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Ecology and Evolution

Much of the work in our lab concerns host-parasite ecology and evolution. We focus mainly on interactions between birds and lice. We are particularly interested in ecological factors that influence the degree of host specificity, population genetic structure, and diversification of lice. These three parameters represent ecological, microevolutionary, and macroevolutionary time. In recent years we have focused largely on Columbiformes (pigeons and doves) and their lice (Figure 1).

 

Fig. 1. Phylogenies for four species of pigeons (uppercase letters) and four species of feather lice (lowercase). Dashed lines show which parasite occurs on which host. The congruence of the two phylogenies shows that the pigeons and lice have speciated in concert, which is known as "cospeciation". For example, splitting of an ancestral pigeon (square) into modern day species A and B was accompanied by splitting of its ancestral louse (star) into modern day species a and b. Note that parasite b is found on host D in addition to host B. This shared host association is the result of a host "switch", in which parasite b jumped to host D (while remaining also on host B).

Experimental Adaptive Radiation - Genomics of Diversification in Bird Lice
(Funded by NSF Dimensions of Biodiversity program)

Adaptive radiations take place when one species of organism splits into several species occupying distinct ecological niches. The process is a common generator of biodiversity, yet the genetic changes underlying it are poorly understood.  Parasites, which represent one of the most diverse groups of organisms on earth, adaptively radiate as they switch to new species of hosts.  We are investigating the genetic architecture of adaptive radiation in parasites.  The focal group consists of feather lice, which are host specific "permanent" parasites that spend all of their time on the host's body. This unusual life cycle makes it possible to study lice under essentially natural conditions even though they are living on captive birds in the lab. This work explores evolutionary changes in parasite size and color, which are fundamental components of successful host use by feather lice.  Different size and color breeds of pigeons (Columba livia) are being used as "stepping stones" to experimentally evolve lice capable of parasitizing hosts on which they do not normally occur in nature.  Genomic changes that accompany the experimental evolution of novel host use are being compared to genomic differences among different species of lice that naturally parasitize different species of pigeons and doves in nature.  The ultimate goal of this work is to integrate across the micro- and macroevolutionary dimensions of evolution in order to transform our understanding of adaptive radiations as a generator of biodiversity.

Body Size 

Fig. 2.  Host and parasite body size are correlated across diverse groups of parasites, a relationship known as "Harrison's Rule".  This size match reinforces host specificity and is thought to play a central role in the speciation and adaptive radiation of parasites among hosts.  For example, Columbicola feather lice of pigeons and doves follow Harrison's Rule.  Larger bird species have coarser feathers with larger barbs and larger spaces in which lice can hide, driving the correlation of host mass and louse size. From Clayton et al. (2003) and Johnson et al. (2005). 

Clayton, D., S. Bush, B. Goates, and K. Johnson. 2003. Host defense reinforces host–parasite cospeciation. Proceedings of the National Academy of Sciences of the United States of America 100: 15694
PDF  Full-text (html)          PDFThe Japan Times   

Johnson, K.P., S.E. Bush, and D.H. Clayton. 2005. Correlated evolution of host and parasite body size: tests of Harrison's rule using birds and lice. Evolution 59(8): 1744–1753.) PDF

Crypsis

Fig. 3. Crypsis in feather lice: the white louse (Neopsittaconirums albus) is a parasite ofthe sulfur-crested cockatoo (Cacatua galerita), the black louse (N. borgiolii) is a parasite of the yellow-tailed black cockatoo (Calyptorhynchus funereus).  Photos of sulfur-crested cockatoo by Fir0002/Flagstaffotos, yellow-tailed black cockatoo by David Cook, and lice by S.E. Bush. From Bush et al. (2010). 

Bush, S.E., D. Kim, M. Reed, and D.H. Clayton. 2010. Evolution of Cryptic Coloration in Ectoparasites. Am Nat 176(4): 529–535. PDF

Crypsis Pigeons

Fig. 4. Crypsis in feather lice of pigeons and doves: the light colored louse (insets: Columbicola wolffhuegeli) is a parasite of the pied imperial pigeon (Ducula bicolor), the dark louse (C. columbae) parasitizes the rock pigeon (Columba livia)Columbicola columbae is the source of the reference genome for this project. Photos of pied imperial pigeon by Fir0002/Flagstaffotos, rock pigeon by Razvan Socol, and lice by S.E. Bush.

  Pigeons

Fig. 5. a) Variation in the sizes of breeds of the Rock pigeon (Columba livia); b) variation in the color of rock pigeons.  Different size and color pigeon breeds will be used as "stepping stone" hosts for experimentally evolving changes in the size and color of Columbicola columbae lice.  These lice will eventually be transferred to different species of pigeons to simulate actual host switches in nature.  Genomic changes associated with the experimental switches will be compared to genomic differences among the different species of lice that have switched to novel host species under natural conditions in the past.

Cophylogenetic

Fig. 6. Cophylogenetic analysis showing significant cospeciation between wing lice (Columbicola) and their pigeon/dove hosts, interspersed with periodic host switching events (e.g. C. theresae to Oena capensis).  Green lines show host-parasite associations.  From Clayton et al. (2003).

Clayton, D., S. Bush, B. Goates, and K. Johnson. 2003. Host defense reinforces host–parasite cospeciation. Proceedings of the National Academy of Sciences of the United States of America 100: 15694
 

Evolutionary Ecology of Columbiform Feather Lice

Past research in the lab focused on understanding the conditions under which parasites are likely to "jump" to new hosts. 

We investigated the determinants of host specificity in pigeons and doves (Columbiformes) that are commonly infested with two different types of lice.  Each host typically has a genus of "wing" louse and a genus of "body" louse. The ecology of wing and body lice is extremely similar; however, they specialize on different regions of the host's body and differ significantly in host specificity (body lice are more specific than wing lice). They also differ significantly in population genetic structure, with body lice showing more structure than wing lice. PDF

We reconstructed phylogenies for the birds and both kinds of lice, using nuclear and mitochondrial DNA sequences that we determine in the lab. Comparisons of the host and parasite trees reveal that body lice have cospeciated more extensively with the host group than wing lice. PDF

We conducted a series of long-term transfer experiments using half a dozen species of North American pigeons and doves that vary substantially in body size, feather size and other features of interest.  The purpose of the transfer experiments was to determine why the two kinds of lice differ in specificity and cospeciation, despite living on the same hosts and having such similar ecologies (e.g. both kinds of lice feed only on feathers located on the host's abdominal region).  We found that wing and body lice were very similar in their ability to establish on novel host species Clayton et al. 2003 Proceedings of the National Academy of Sciences, USA. PDF

So, why do body lice show greater specificity and cospeciation than wing lice? The answer will has little to do with the ability of lice to establish on novel hosts, and more to do with the ability of lice to disperse among different species of hosts. The relative fitness of permanent parasites on novel hosts is of little importance if the parasites never have an opportunity to reach those hosts. To address this issue we conducted series of experiments designed to measure the relative ability of wing and body lice to disperse between hosts by hitchhiking phoretically on non-specific parasitic flies (Figure 7).  Our experiments showed that wing lice readily engaged in phoretic transmission between individual birds, and host species. In contrast, body lice are not phoretic.   

Harbison, C.W., S.E. Bush, J.R. Malenke, and Dale H. Clayton. 2008. Comparative transmission dynamics of competing parasite species. Ecology 89:3186-3194. PDF

Harbison, C. W. and D. H. Clayton. 2011. Community interactions govern host-switching with implications for host-parasite coevolutionary history. PNAS 108: 9525-9529.PDF

These results underscore the importance of a broad community approach to understanding the complex nature of transmission and host specificity.

Fig. 7. Three feather lice (Columbicola columbae) hitchhiking phoretically on a parasitic hippoboscid fly (Pseudolynchia canariensis). (Illustrated from an actual case by Sarah E. Bush)

Work on bird-louse cospeciation is relevant to host-parasite systems, in general. The work even has relevance to human health because it can help us to develop a solid conceptual approach for predicting conditions under which host-specific parasites may move to new species of hosts. For example, the HIV virus evolved as a result of a host switch from non-human primates to humans. What governs the probability of such switches? This question is also important for assessing the health and well being of domesticated animals and wildlife, including endangered species at risk of pathogen-mediated extinction. In summary, we aretrying to develop a general research program to address the coevolution of host-specific parasites and pathogens.

Evolutionary Ecology of Other Host-parasite Interactions

We are also interested other kinds of host-parasite interaction, such as that between birds and malarial blood parasites.  To date, this work has involved experiments with pigeons, hippoboscid flies and Haemoproteus columbae, an apicomlexan blood parasite that uses the flies as vectors and pigeons as the final hosts.  We recently published our first two papers on this system:


Knutie, S. A., J. L. Waite and D. H. Clayton.  2012.  Does avian malaria reduce host fledging success:  A test of the "selection" hypothesis.  Evolutionary Ecology. DOI    10.1007/s10682-012-9578-y PDF


Waite, J. L., A. R. Henry, F, R. Adler and D. H. Clayton.  2012. Sex-specific effects of avian malaria on an insect vector:  Support for the resource limitation hypothesis.  Ecology 93: 2448–2455. PDF

We are also deeply involved in work on an invasive parasitic nest fly of Darwin's Finches in the Galapagos Islands.  For a description of this work see the Conservation section of our website.