Ben C. Sheldon

Ecological immunology : Costly parasite defences and trade-offs in evolutionary ecology

In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individuals immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.

Differential allocation: tests, mechanisms and implications

Differential allocation occurs when reproductive investment is influenced by mate attractiveness. Recently, wide-ranging empirical support for differential allocation has been obtained. These data suggest that mates can affect the payoffs from reproduction, thus making sacrifices of reproductive value worthwhile when breeding with an attractive mate. As an example of an adaptive parental effect, the existence of differential allocation has some interesting implications for empirical studies of sexual selection and for predicting evolutionary responses to selection.

Infectious diseases, reproductive effort and the cost of reproduction in birds

Reproductive effort can have profound effects on subsequent performance. Field experiments on the collared flycatcher (Ficedula albicollis) have demonstrated a number of trade-offs between life-history traits at different ages. The mechanism by which reproductive effort is mediated into future reproductive performance remains obscure. Anti-parasite adaptation such as cell-mediated immunity may probably also be costly. Hence the possibility exists of a trade-off between reproductive effort and the ability to resist parasitic infection. Serological tests on unmanipulated collared flycatchers show that pre-breeding nutritional status correlates positively with reproductive success and negatively with susceptibility to parasitism (viruses, bacteria and protozoan parasites). Both immune response and several indicators of infectious disease correlate negatively with reproductive success. Similar relations are found between secondary sexual characters and infection parameters. For brood-size-manipulated birds there was a significant interaction between experimentally increased reproductive effort and parasitic infection rate with regard to both current and future fecundity. It seems possible that the interaction between parasitic infection, nutrition and reproductive effort can be an important mechanism in the ultimate shaping of life-history variation in avian populations.

Genetic architecture of fitness and nonfitness traits : empirical patterns and development of ideas

Comparative studies of the genetic architecture of different types of traits were initially prompted by the expectation that traits under strong directional selection (fitness traits) should have lower levels of genetic variability than those mainly under weak stabilizing selection (nonfitness traits). Hence, early comparative studies revealing lower heritabilities of fitness than nonfitness traits were first framed in terms of giving empirical support for this prediction, but subsequent treatments have effectively reversed this view. Fitness traits seem to have higher levels of additive genetic variance than nonfitness traits — an observation that has been explained in terms of the larger number loci influencing fitness as compared to nonfitness traits. This hypothesis about the larger functional architecture of fitness than nonfitness traits is supported by their higher mutational variability, which is hard to reconcile without evoking capture of mutational variability over many loci. The lower heritabilities of fitness than nonfitness traits, despite the higher additive genetic variance of the former, occur because of their higher residual variances. Recent comparative studies of dominance contributions for different types of traits, together with theoretical predictions and a large body of indirect evidence, suggest an important role of dominance variance in determining levels of residual variance for fitness-traits. The role of epistasis should not be discounted either, since a large number of loci increases the potential for epistatic interactions, and epistasis is strongly implicated in hybrid breakdown.

Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds

In field and laboratory studies of birds, positive associations between male phenotype and success at obtaining extra-pair copulations or extra-pair fertilizations are often interpreted as providing evidence that females are using extra-pair copulations to obtain indirect benefits for their offspring, either through genes for increased viability, or for a fisherian mating advantage. I describe a simple model, in which functional fertility (the success of ejaculates in fertilizing eggs) covaries with male phenotype, which can explain the observed associations equally well. Under such a model, females pursue extra-pair copulations as insurance against the functional infertility of their mate, and obtain only direct benefits for themselves in their current reproductive event. Several studies of birds suggest that a relation between male phenotype and functional fertility is often likely to exist and that there are many potential causes of functional infertility. Non-manipulative field studies are unlikely to produce results which distinguish between the two hypotheses, and I discuss several alternative approaches which may allow their resolution.

Sexual selection resulting from extrapair paternity in collared flycatchers.

Extrapair paternity has been suggested to represent a potentially important source of sexual selection on male secondary sexual characters, particularly in birds with predominantly socially monogamous mating systems. However, relatively few studies have demonstrated sexual selection within single species by this mechanism, and there have been few attempts to assess the importance of extrapair paternity in relation to other mechanisms of sexual selection. We report estimates of sexual selection gradients on male secondary sexual plumage characters resulting from extrapair paternity in the collared flycatcher Ficedula albicollis, and compare the importance of this form of sexual selection with that resulting from variation in mate fecundity. Microsatellite genotyping revealed that 15% of nestlings, distributed nonrandomly among 33% of broods (N=79), were the result of extrapair copulations. Multivariate selection analyses revealed significant positive directional sexual selection on two uncorrelated secondary sexual characters in males (forehead and wing patch size) when fledgling number was used as the measure of fitness. When number of offspring recruiting to the breeding population was used as the measure of male fitness, selection on these traits appeared to be directional and stabilizing, respectively. Pairwise comparisons of cuckolded and cuckolding males revealed that males that sired young through extrapair copulations had wider forehead patches, and were paired to females that bred earlier, than the males that they cuckolded. Path analysis was used to partition selection on these traits into pathways via mate fecundity and sperm competition, and suggested that the sperm competition pathway accounted for between 64 and 90% of the total sexual selection via the two paths. The selection revealed in these analyses is relatively weak in comparison with many other measures of selection in natural populations. We offer some explanations for the relatively weak selection detected. Copyright 1999 The Association for the Study of Animal Behaviour.

New tools for sex identification and the study of sex allocation in birds.

The recent development of simple, DNA-based methods for the determination of an individuals sex will make possible large-scale studies of sex allocation and the consequence of gender in birds. Birds provide ideal systems for studying these questions in vertebrates, as so much is known about their biology and determinants of fitness. Until recently, however, little quantitative work has been possible because of the difficulty in determining gender in most cases. Recent studies suggest that biased sex allocation be more widespread in birds than has been realized.

Recent studies of avian sex ratios

Sex allocation theory, and its success in predicting sex ratios in such taxa as parasitoid wasps, is often cited as one of the crowning achievements of theoretical evolutionary biology. Its success in some vertebrate taxa, particularly birds, has been more modest. I discuss two reasons for this. First, it is difficult to obtain avian sex ratio data before substantial offspring mortality has occurred. Second, the theory and data required to predict sex allocation patterns (let alone sex ratio patterns) in vertebrates are complex and hard to obtain. Recently developed molecular genetic techniques allowing sex identification from DNA samples have largely solved the first problem and there have been several striking empirical demonstrations of sex ratio biases consistent with sex allocation theory in wild bird populations. Solution of the second problem may come with the incorporation of realistic life history data into models and the use of experimental manipulations to reveal the fitness consequences of allocation strategies. Further data concerning sex ratio variation in taxa such as birds, with chromosomal sex determination, are valuable because they allow the investigation of the role of constraint vs. adaptation in evolution.

Why do male birds not discriminate between their own and extra-pair offspring?

Abstract A number of recent models of optimal paternal investment predict that males should alter their investment in offspring in response to changes in paternity or certainty of paternity. One way in which it has been suggested that male birds might do this would be to recognize their own offspring and to discriminate in their favour. Despite frequent statements that nothing is known about whether birds possess this ability or whether they exercise it, there is a considerable body of evidence suggesting that males do not discriminate against non-related offspring. This evidence is reviewed and an attempt made to explain the absence of kin discrimination in males under these circumstances by considering potential mechanisms of kin discrimination. Although there is selection for males to discriminate in favour of their own offspring it is argued that they are unable to do so because of conflicts between the male, female and offspring over signalling identity, and because the circumstances associated with extra-pair paternity disrupt the operation of some mechanisms. Male birds might possess behavioural ‘rules of thumb’ which lead to behaviour that appears similar to offspring recognition, but the sophistication of such rules is likely to be limited by the stochasticity inherent in fertilization.

Testis size variation in the greenfinch Carduelis chloris : relevance for some recent models of sexual selection

Abstract Interspecific evidence that testis size responds to selection caused by sperm competition has been obtained from many taxa. However, little is known about the sources of intraspecific variation in testis size, although such variation may have functional significance. Variation in testis size and asymmetry was studied within and between eight geographically separated (and genetically differentiated) populations of greenfinches Carduelis chloris. The relationships between testis size and plumage brightness (degree of yellowness) and the prevalence of haematozoan infections were also investigated in three of these populations, as they related to the predictions of the immunocompetence handicap hypothesis, and Møllers hypothesis relating directional testis asymmetry to phenotypic quality. There were large differences between populations in testis size, with males from northern populations having larger testes than those from southern populations. Within populations, large testes were associated with larger body size and greater age. When the influence of these factors was removed statistically, males with large testes were more likely to be infected with haematozoan parasites, and had brighter yellow plumage. No evidence was found that directional asymmetry in testis size was related to either of these measures of phenotypic quality. These results are consistent with the hypothesis that males with large testes, while signalling higher phenotypic quality as revealed by increased plumage brightness, also pay a cost in terms of reduced immunocompetence, revealed by the increased probability of infection in these males. That these patterns were similar in three different populations adds further strength to these conclusions. Our results suggest that studying the sources of variation in testis size among individuals can reveal interesting processes in sexual selection.