Alternative hypotheses linking the immune system and mate choice for good genes

Why do males often have extravagant morphological and behavioural traits, and why do females prefer to mate with such males? The answers have been the focus of considerable debate since Darwin's 'The descent of man, and selection in relation to sex' appeared in 1871. Recently, the broadening of investigation to include fields outside evolutionary biology has shed new light on mate choice and sexual selection. Here, we focus on a specific set of hypotheses relating the biology of resisting disease-causing organisms with the production of condition-dependent sexual signals (advertisements). We present a framework that distinguishes three different hypotheses about trade-offs within the immune system that affect general condition. The original Hamilton & Zuk hypothesis suggests that hosts fight off disease via resistance to particular pathogens, which lowers resistance to other pathogens. Changes in pathogens over evolutionary time in turn favours changes in which genes confer the best resistance. Alternatively, the immunocompetence hypotheses suggest that the energetic costs of mounting a response to any pathogen compete for resources with other things, such as producing or maintaining advertisements. Finally, improving resistance to pathogens could increase the negative impacts of the immune system on the host, via immunopathologies such as allergies or autoimmune diseases. If both disease and immunopathology affect condition, then sexual advertisements could signal a balance between the two. Studies of hypothesized links between genes, condition, the immune system and advertisements will require careful consideration of which hypothesis is being considered, and may necessitate different measures of immune system responses and different experimental protocols

Simple sequence repeats in zebra finch (Taeniopygia guttata) expressed sequence tags: a new resource for evolutionary genetic studies of passerines

Background Passerines (perching birds) are widely studied across many biological disciplines including ecology, population biology, neurobiology, behavioural ecology and evolutionary biology. However, understanding the molecular basis of relevant traits is hampered by the paucity of passerine genomics tools. Efforts to address this problem are underway, and the zebra finch (Taeniopygia guttata) will be the first passerine to have its genome sequenced. Here we describe a bioinformatic analysis of zebra finch expressed sequence tag (EST) Genbank entries. Results A total of 48,862 ESTs were downloaded from GenBank and assembled into contigs, representing an estimated 17,404 unique sequences. The unique sequence set contained 638 simple sequence repeats (SSRs) or microsatellites of length ≥20 bp and purity ≥90% and 144 simple sequence repeats of length ≥30 bp. A chromosomal location for the majority of SSRs was predicted by BLASTing against assembly 2.1 of the chicken genome sequence. The relative exonic location (5' untranslated region, coding region or 3' untranslated region) was predicted for 218 of the SSRs, by BLAST search against the ENSEMBL chicken peptide database. Ten loci were examined for polymorphism in two zebra finch populations and two populations of a distantly related passerine, the house sparrow Passer domesticus. Linkage was confirmed for four loci that were predicted to reside on the passerine homologue of chicken chromosome 7. Conclusion We show that SSRs are abundant within zebra finch ESTs, and that their genomic location can be predicted from sequence similarity with the assembled chicken genome sequence. We demonstrate that a useful proportion of zebra finch EST-SSRs are likely to be polymorphic, and that they can be used to build a linkage map. Finally, we show that many zebra finch EST-SSRs are likely to be useful in evolutionary genetic studies of other passerines

Testes asymmetry, condition and sexual selection in birds: an experimental test

The functional significance of the marked directional asymmetry in testes size observed in many bird species is obscure. Møller suggested that (i) the smaller of the two testes serves a compensatory role and increases in size (and hence reduces asymmetry) when the larger one is defective in some way, and (ii) as a consequence, the degree of directional asymmetry in testes size reflects male quality and covaries positively with the expression of secondary sexual traits.We conducted an experimental test of these two hypotheses in the zebra finch,Taeniopygia guttata. Neither hypothesis was supported. First, there was no significant relationship between the size of the left testis and relative testes asymmetry. Second, we obtained no support for the hypothesis that the degree of directional asymmetry in testes mass covaried with condition. On the contrary, directional asymmetry in testes mass was signifcantly greater in birds whose condition was experimentally reduced, compared with control birds. Moreover, we found no significant relationships between testes asymmetry and secondary sexual traits. We conclude that directional asymmetry in testes size does not reflect male condition in the zebra finch

Sperm competition and sperm midpiece size: no consistent pattern in passerine birds

Sperm competition is thought to be a major force driving the evolution of sperm shape and function. However, previous studies investigating the relationship between the risk of sperm competition and sperm morphometry revealed inconclusive results and marked differences between taxonomic groups. In a comparative study of two families of passerines (Fringillidae and Sylviidae) and also across species belonging to different passerine families, we investigated the relative importance of the phylogenetic background on the relationship between sperm morphometry and the risk of sperm competition. The risk of sperm competition was inferred from relative testis mass as an indicator of investment in sperm production. We found: (i) a significant positive association between both midpiece length and flagellum length and relative testis mass in the Fringillidae, (ii) a significant negative association between sperm trait dimensions and relative testis mass in the Sylviidae, and (iii) no association across all species. Despite the striking difference in the patterns shown by the Sylviidae and the Fringillidae, the relationship between midpiece length and flagellum length was positive in both families and across all species with positive allometry. Reasons for the differences and similarities between passerine families are discussed

The identity of the bird known locally in sixteenth- and seventeenth-century Norfolk, United Kingdom, as the Spowe

In the kitchen record books of the L'Estrange family in the sixteenth and seventeenth centuries, there are references to a bird, widely shot on the Norfolk coast, called a Spowe. On the basis of the similarity to the Icelandic name, J. H. Gurney (sen.) and Fisher (in their "An account of birds found in Norfolk" published in 1846) assumed this to be the Whimbrel (Numenius phaeopus) as have all ornithological texts ever since. Internal evidence from the kitchen records strongly suggest that the Spowe was a winter visitor, not a passage migrant, thus throwing considerable doubt on Gurney and Fisher's ascription. We suggest that it is much more likely that the Spowe was the Bar-tailed Godwit (Limosa lapponica)

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour

The insemination window provides a distorted view of sperm competition in birds

The aim of this study is to identify and rectify a misunderstanding about the optimal timing of inseminations in birds. In species laying clutches of more that one egg, a copulation during the hour following egg-laying can result in sperm reaching the site of fertilization in time to fertilize the next egg to be laid. Cheng et al. (1983) referred to this period as the insemination window and proposed that it was an 'espcially favourable period' for males to obtain extra-pair copulations. As stated in their paper, this is true only in terms of the next ovum to be fertilized, but subsequent authors assumed that the insemination window represents a general peak in female fertility and have made predictions about the optimal timing of extra-pair behaviours and paternity guards relative to it. Far from being a general peak in female fertilty, we show by a re-analysis of Cheng et al.s data and by using published information on the domestic fowl Gallus domesticus, turkey Gallopavo meleagris and Muscovy duck Cairina Moschata, that inseminations either just after egg laying or just before it are much less likely overall to result in fertilization than inseminations made at other times. The reduced efficacy of inseminations made close to the time of egg-laying occurs because the retention of sperm by females inseminated at this time is low. The fact that inseminations made around the time of the egg laying in the domestic fowl, turkey and Muscovy duck have a reduced probability of fertilization is consistent with the fact that very few wild birds,even those in which sperm competition is intense, alter their copulation or mate guarding behaviour during the insemination window

Sperm precedence in the domestic fowl

The aim of this study was to examine last-male sperm precedence in the domestic fowl. We used sperm from two different genotypes to assign paternity: and in seven experiments females were artificially inseminated with either equal or unequal numbers of sperm at intervals of 4 or 24 h. We were unable to replicate the results of a previous study by Compton et al. (1978) in which a strong last-male precedence effect had been recorded when two equal sized inseminations were made 4 h apart. We observed no marked last-male sperm precedence and our results did not differ significantly from that predicted by the passive sperm loss model, in which a last-male effect is determined by the rate at which sperm are lost from the female tract and the interval between successive inseminations. The most likely explanation for the disparity between our result and Compton et al.'s is a difference in the timing of inseminations. The implications of this for studies of sperm competition in birds is discussed

Sperm precedence in zebra finches does not require special mechanisms of sperm competition

Competition between the spermatozoa of different males to fertilize the eggs of a single female acts as a selection pressure on the behaviour of males and females. However, quantitative predictions about behaviour fan only be made if the paternity consequences of different patterns of copulation are known. Because exhaustive empirical measurement of these consequences may be impractical, interest has centred on determining the mechanisms by which sperm competition occurs, knowledge of which may allow consequences to be calculated. One method of elucidating mechanisms of sperm competition is to use mathematical models to determine which mechanisms are necessary or sufficient to account for empirical observations. We use this approach for zebra finches Taeniopygia guttata and show that empirically measured rates of disappearance of sperm from the reproductive tract, and differences in the number of sperm in the first and subsequent ejaculates of each male, are sufficient to account for observed levels of sperm precedence. Special mechanisms of sperm competition, such as displacement or stratification of sperm, are therefore unnecessary to explain sperm precedence in this species