Dale H. Clayton

Experimental Demonstration of the Energetic Cost of Parasitism in Free-Ranging Hosts

Although some parasites have obvious pathogenic effects, others appear to have subtle, indirect effects that are poorly understood, particularly in natural populations. Indirect effects may result from parasites altering host metabolic rate and hence host energy needs, yet no experimental studies have shown this to be the case for non-laboratory hosts. We report the results of a long-term field experiment designed to test the impact of parasites on host energetics. We measured the energetics of feral rock doves ( with populations of feather-feeding lice, traditionally considered to have little or no effect on host fitness. The lice reduced feather mass leading to increased thermal conductance and metabolic rate, as well as a steady reduction in host body mass over the course of the nine-month study. Our results demonstrate that even classically ‘benign’ parasites such as feather lice can reduce host condition through the accumulation of subtle energetic costs over time. We argue that experimental manipulations are a prerequisite for documenting such effects.

Sampling Effort and Parasite Species Richness

Comparative studies of parasite species richness among host taxa can be confounded by uneven sampling effort. Sampling ceases to be a confounding factor when extrapolation methods are used to estimate true species richness. Here, Bruno Walther and colleagues review examples of sampling bias and the use of extrapolation methods for circumventing it. They also discuss the confounding effects of phylogenetic association of estimates of species richness.

Genetic analysis of lice supports direct contact between modern and archaic humans.

Parasites can be used as unique markers to investigate host evolutionary history, independent of host data. Here we show that modern human head lice, Pediculus humanus, are composed of two ancient lineages, whose origin predates modern Homo sapiens by an order of magnitude (ca. 1.18 million years). One of the two louse lineages has a worldwide distribution and appears to have undergone a population bottleneck ca. 100,000 years ago along with its modern H. sapiens host. Phylogenetic and population genetic data suggest that the other lineage, found only in the New World, has remained isolated from the worldwide lineage for the last 1.18 million years. The ancient divergence between these two lice is contemporaneous with splits among early species of Homo, and cospeciation analyses suggest that the two louse lineages codiverged with a now extinct species of Homo and the lineage leading to modern H. sapiens. If these lice indeed codiverged with their hosts ca. 1.18 million years ago, then a recent host switch from an archaic species of Homo to modern H. sapiens is required to explain the occurrence of both lineages on modern H. sapiens. Such a host switch would require direct physical contact between modern and archaic forms of Homo.

Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera)

Five methods for estimating the abundance of chewing lice (Insecta: Phthiraptera) were tested. To evaluate the methods, feral pigeons (Columba livia) and 2 species of ischnoceran lice were used. The fraction of lice removed by each method was compared, and least squares linear regression was used to determine how well each method predicted total abundance. Total abundance was assessed in most cases using KOH dissolution. The 2 methods involving dead birds (body washing and post-mortem-ruffling) provided better results than 3 methods involving live birds (dust-ruffling, fumigation chambers, and visual examination). Body washing removed the largest fraction of lice (>82%) and was an extremely accurate predictor of total abundance (r2 = 0.99). Post-mortem-ruffling was also an accurate predictor of total abundance (r2 ≥ 0.88), even though it removed a smaller proportion of lice (<70%) than body washing. Dust-ruffling and fumigation chambers removed even fewer lice, but were still reasonably accurate predictors of total abundance, except in the case of data sets restricted to birds with relatively few lice. Visual examination, the only method not requiring that lice be removed from the host, was an accurate predictor of louse abundance, except in the case of wing lice on lightly parasitized birds.

Ectoparasite Virulence is Linked to Mode of Transmission

Theory suggests that the evolution of parasite virulence is linked to the dynamics of parasite transmission. All else being equal, parasites transmitted vertically from parents to offspring should be less virulent than parasites capable of horizontal transmission to unrelated hosts. This is because the fitness of vertically transmitted parasites is tightly linked to the reproductive success of the host, whereas the fitness of horizontally transmitted parasites is relatively independent of host reproduction. The virulence-transmission relation has seldom been tested because of difficulties inherent in comparing virulences of different parasite-host systems. We compared the virulence of lice and mites infesting a single group of captive rock doves (Columba livia). Lice, which were vertically transmitted, had no detectable effect on host fitness, whereas horizontally transmitted mites drove host reproductive success to zero. These results, in conjunction with a survey of the literature, support the hypothesis that ectoparasite virulence is linked to the mode of transmission.

Reciprocal Natural Selection on Host‐Parasite Phenotypes

Coevolution is evolution in one species in response to selection imposed by a second species, followed by evolution in the second species in response to reciprocal selection imposed by the first species. Although reciprocal selection is a prerequisite of coevolution, it has seldom been documented in natural populations. We examined the feasibility of reciprocal selection in a simple host‐parasite system consisting of feral pigeons (Columba livia) and their Ischnoceran feather lice (Phthiraptera: Insecta). We tested for a selective effect of parasites on hosts with experimentally altered defenses and for a selective effect of host defense on a component of parasite escape. Previous work indicates that pigeons control lice through efficient preening, while lice escape from preening using complex avoidance behavior. Our results show that feral pigeons with impaired preening, owing to slight bill deformities, have higher louse loads than pigeons with normal bills. We use a controlled experiment to show that high louse loads reduce the survival of pigeons, suggesting that lice select for efficient preening and against bill deformities. In a reciprocal experiment, we demonstrate that preening with a normal bill selects for small body size in lice, which may facilitate their escape from preening. The results of this study verify a crucial element of coevolutionary theory by identifying likely targets of reciprocal phenotypic selection between host and parasite.

The population genetics of host specificity: genetic differentiation in dove lice (Insecta : Phthiraptera)

Some species of parasites occur on a wide range of hosts while others are restricted to one or a few host species. The host specificity of a parasite species is determined, in part, by its ability to disperse between host species. Dispersal limitations can be studied by exploring the genetic structure of parasite populations both within a single species of host and across multiple host species. In this study we examined the genetic structure in the mitochondrial cytochrome oxidase I (COI) gene of two genera of lice (Insecta: Phthiraptera) occurring on multiple sympatric species of doves in southern North and Central America. One genus, Columbicola, is generally less host‐specific than the other, Physconelloides. For both genera we identified substantial genetic differentiation between populations of conspecific lice on different host species, generally 10–20% sequence divergence. This level of divergence is in the range of that often observed between species of these two genera. We used nested clade analysis to explore fine scale genetic structure within species of these feather lice. We found that species of Physconelloides exhibited more genetic structure, both among hosts and among geographical localities, than did species of Columbicola. In many cases, single haplotypes within species of Columbicola are distributed on multiple host species. Thus, the population genetic structure of species of Physconelloides reveals evidence of geographical differentiation on top of high host species specificity. Underlying differences in dispersal biology probably explain the differences in population genetic structure that we observed between Columbicola and Physconelloides.

How Birds Combat Ectoparasites

Birds are plagued by an impressive diversity of ectoparasites, ranging from feather-feeding lice, to feather- degrading bacteria. Many of these ectoparasites have severe negative effects on host fitness. It is therefore not surprising that selection on birds has favored a variety of possible adaptations for dealing with ectoparasites. The functional signifi- cance of some of these defenses has been well documented. Others have barely been studied, much less tested rigorously. In this article we review the evidence - or lack thereof - for many of the purported mechanisms birds have for dealing with ectoparasites. We concentrate on features of the plumage and its components, as well as anti-parasite behaviors. In some cases, we present original data from our own recent work. We make recommendations for future studies that could im- prove our understanding of this poorly known aspect of avian biology.

The adaptive significance of self-medication

Not all pharmacists are human; other species also use medicinal substances to combat pathogens and other parasites. Self-medicating behaviour is a topic of rapidly growing interest to behaviourists, parasitologists, ethnobotanists, chemical ecologists, conservationists and physicians. Although most of the pertinent literature is anecdotal, several studies have now attempted to test the adaptive function of particular self-medicating behaviours. We discuss the results of these studies in relation to simple hypotheses that can provide a framework for future tests of self-medication.

When Do Parasites Fail to Speciate in Response to Host Speciation

Cospeciation generally increases the similarity between host and parasite phylogenies. Incongruence between host and parasite phylogenies has previously been explained in terms of host switching, sorting, and duplication events. Here, we describe an additional process, failure of the parasite to speciate in response to host speciation, that may be important in some host-parasite systems. Failure to speciate is likely to occur when gene flow among parasite populations is much higher than that of their hosts. We reconstructed trees from mitochondrial and nuclear DNA sequences for pigeons and doves (Aves: Columbiformes) and their feather lice in the genus Columbicola (Insecta: Phthiraptera). Although comparisons of the trees from each group revealed a significant amount of cospeciation, there was also a significant degree of incongruence. Cophylogenetic analyses generally indicated that host switching may be an important process in the history of this host-parasite association. Using terminal sister taxon comparisons, we also identified three apparent cases where the host has speciated but the associated parasite has not. In two of these cases of failure to speciate, these comparisons involve allopatric sister taxa of hosts whose lice also occur on hosts sympatric with both of the allopatric sisters. These additional hosts for generalist lice may promote gene flow with lice on the allopatric sister species. Relative rate comparisons for the mitochondrial cytochrome oxidase I gene indicate that molecular substitution occurs about 11 times faster in lice than in their avian hosts.