Ecology
Much of the work in our lab concerns host-parasite ecology. 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 phylogenetic congruence between birds and 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).
Figure 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).We are simulating such host switches by moving lice among species of captive pigeons and doves in controlled experiments. One goal of this work is to predict the conditions under which parasites are likely to "jump" to new hosts. We have conducted a series of long-term transfer experiments using half a dozen species of North American pigeons and doves. These species vary substantially in body size, feather size and other features of interest. Each 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 (Johnson et al. 2002 Molecular Ecology).
In conjunction with our transfer experiments, we have reconstructing 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 (Clayton and Johnson 2003 Evolution).
The purpose of the transfer experiments is 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). Our preliminary results show that both kinds of lice have low relative fitness when transferred to hosts that differ from the native host in body size.
Why is size so important? We have also conducted a series of experiments to test three possible adaptive hypotheses:
1. Attachment -- the ability of lice to hold onto feathers of various sizes.
2. Feeding -- the ability of lice to feed on feathers of various sizes.
3. Escape -- the ability of lice to escape host defense (preening) on different feathers.Our results show that lice are capable of holding onto, and feeding upon, feathers of many different sizes. In contrast, our results show that lice are unable to escape from preening on feathers of different sizes (Clayton et al. 2003 Proceedings of the National Academy of Sciences, USA ).
We are currently comparing the specific escape performance of lice on feathers of different sizes to understand exactly how size influences escape.
But what about the original question as to why body lice show greater specificity and cospeciation than wing lice? We haven't yet answered this question, although it is beginning to look as though the answer will have 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 have recently begun a 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 2).
Figure 2. 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 are trying to develop a general research program to address the coevolution of host-specific parasites and pathogens.
NEW PROJECT: Co-evolutionary ecology of Darwin's Finches and parasites
Figure 3. Darwin's Finches and ectoparasites: a) Adult fly (Philornis sp.), parasitic stage is the larvae; b) Bird louse (Brueelia sp.); c) Feather mite (Mesalgoides sp.); d) Small ground finch (Geospiza fuliginosa); e) Medium ground finch (G. fortis) – in shaded circle - is focus of most of our work; f) Large ground finch (G. magnirostris); g) Large cactus finch (G. conirostris); h) Common cactus finch (G. scandens); i) Sharp-beaked ground finch, (G. difficilis); j) Woodpecker finch (Cactospiza pallida); k) Small tree finch (Cam. parvulus); l) Large tree finch (Cam. psittacula); m) Vegetarian finch (Platyspiza crassirostris); n) “central islands” Warbler finch (Certhidea olivacea); o) “outer islands” Warbler finch (Cer. fusca).
This new project, which is based in Utah and the Galapagos Islands, is at the interface of co-evolutionary ecology, immunology, behavior, and conservation biology. Although Darwin’s Finches are one of the most famous examples of adaptive radiation (Figure 3), we know little about the role of parasites in their ecology, behavior and evolution. Unfortunately, finch populations have recently come under serious threat from the introduced tropical nest fly Philornis downsi. A better understanding of this parasite is urgently needed because of the danger it poses to these iconic birds. The overriding goals of this project are: 1) to conduct rigorous tests of the impact of P. downsi and other parasites on Darwin's Finches, and 2) to determine the ability of the finches to defend themselves against parasites. The project will focus on interactions between P. downsi and the Medium ground finch (Geospiza fortis) on Santa Cruz Island; however, we will also study interactions between other species of finches and their ectoparasite communities (Figure 3). We hope that this work will help conservation biologists protect Darwin's Finches from invasive parasites and pathogens in the future.
