Sperm numbers as a paternity guard in a wild bird

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success

No Evidence for Pre-Copulatory Sexual Selection on Sperm Length in a Passerine Bird

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection

Species-level divergences in multiple functional traits between the two endemic subspecies of Blue Chaffinches Fringilla teydea in Canary Islands

Background: One of the biggest challenges in avian taxonomy is the delimitation of allopatric species because their reproductive incompatibility cannot be directly studied in the wild. Instead, reproductive incompatibility has to be inferred from multiple, divergent character sets that indicate a low likelihood of allopatric populations amalgamating upon secondary contact. A set of quantitative criteria for species delimitation has been developed for avian taxonomy. Results: Here, we report a broad multi-trait comparison of the two insular subspecies of the Blue Chaffinch Fringilla teydea, endemic to the pine forests of Tenerife (ssp. teydea) and Gran Canaria (ssp. polatzeki) in the Canary Islands. We found that the two taxa were reciprocally monophyletic in their whole mitogenomes and two Z chromosome introns. The genetic distance in mitogenomes indicates around 1 Mya of allopatric evolution. There were diagnostic differences in body morphometrics, song and plumage reflectance spectra, whose combined divergence score (=11) exceeds the threshold level (=7) set for species delimitation by Tobias et al. (Ibis 152:724–746, 2010). Moreover, we found a marked divergence in sperm lengths with little range overlap. Relatively long sperm with low intra- and intermale CV compared to other passerines suggest a mating system with high levels of sperm competition (extrapair paternity) in these taxa. Conclusion: The large and diagnostic divergences in multiple functional traits qualify for species rank, i.e., Tenerife Blue Chaffinch (Fringilla teydea) and Gran Canaria Blue Chaffinch (Fringilla polatzeki). We encourage a wider use of sperm traits in avian taxonomy because sperm divergences might signal reproductive incompatibility at the postcopulatory prezygotic stage, especially in species with sperm competition

Endless forms of sexual selection

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a "stock-taking\u27\u27 workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the \u27aesthetic sense\u27 proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate \u27null model\u27 of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress

Sperm Length Variation as a Predictor of Extrapair Paternity in Passerine Birds

The rate of extrapair paternity is a commonly used index for the risk of sperm competition in birds, but paternity data exist for only a few percent of the approximately 10400 extant species. As paternity analyses require extensive field sampling and costly lab work, species coverage in this field will probably not improve much in the foreseeable future. Recent findings from passerine birds, which constitute the largest avian order (∼5,900 species), suggest that sperm phenotypes carry a signature of sperm competition. Here we examine how well standardized measures of sperm length variation can predict the rate of extrapair paternity in passerine birds.We collected sperm samples from 55 passerine species in Canada and Europe for which extrapair paternity rates were already available from either the same (n = 24) or a different (n = 31) study population. We measured the total length of individual spermatozoa and found that both the coefficient of between-male variation (CV(bm)) and within-male variation (CV(wm)) in sperm length were strong predictors of the rate of extrapair paternity, explaining as much as 65% and 58%, respectively, of the variation in extrapair paternity among species. However, only the CV(bm) predictor was independent of phylogeny, which implies that it can readily be converted into a currency of extrapair paternity without the need for phylogenetic correction.We propose the CV(bm) index as an alternative measure to extrapair paternity for passerine birds. Given the ease of sperm extraction from male birds in breeding condition, and a modest number of sampled males required for a robust estimate, this new index holds a great potential for mapping the risk of sperm competition across a wide range of passerine birds

The use of blue tit eggs as a biomonitoring tool for organohalogenated pollutants in the European environment

In the present study, large scale geographical variation in the occurrence of organohalogenated pollutants (OHPs) was investigated throughout Europe using eggs of a terrestrial resident passerine species, the blue tit (Cyanistes caeruleus). Blue tit eggs from 10 sampling locations, involving suburban, rural and remote areas, in 7 European countries were collected and analysed. Sum polychlorinated biphenyl (PCB) levels ranged from 150 ng/g lipid weight (lw) to 2003 ng/g lw. Sum polybrominated diphenyl ethers (PBDEs) ranged from 3.95 ng/g lw to 114 ng/g lw. As expected, PCB and PBDE concentrations were significantly higher in the sampled suburban locations compared to the rural and remote locations. Sum organochlorine pesticides (OCPs) ranged from 122 ng/g lw to 775 ng/g lw. OCP concentrations were, against the expectations, found to be lower in the rural sampling locations compared to the other locations. Contamination profiles of PCBs, PBDEs and OCPs differed also among the sampling locations, which may be due to local contamination sources. Finally, we compared the results of this study with previously reported OHP concentrations in the eggs of a closely related species, the great tit (Parus major), from the same sampling locations in Europe. We found no differences in concentrations between the species. In addition, we found a significant, positive correlation between the sum PCB concentrations in blue tit eggs and great tit eggs, suggesting similar exposure pathways, mechanisms of accumulation and maternal transfer of PCBs. In conclusion, our results suggest the usefulness of eggs from passerine birds as a biomonitoring tool for OHPs on a large geographical scale.Peer reviewe

Age-dependent relationships between multiple sexual pigments and condition in males and females

The reliability of sexual signaling may change across age classes due to shifts in resource allocation patterns. Two contrasting hypotheses exist regarding how the condition dependence of ornaments may shift with age, and both have received empirical support. On one hand, ornaments may more reliably reflect condition and quality in older individuals, because younger individuals of high quality invest in survival over signaling effort. On the other hand, the condition dependence of ornaments may decline with age, if older individuals in poor condition terminally invest in ornaments, or if resource constraints decline with age. Further, the expression and condition dependence of different ornaments may shift with age in unique ways, such that multifaceted sexual displays maintain reliable signaling across age classes. In yellow warblers (Setophaga petechia) of both sexes, we assessed how relationships between carotenoid-and phaeomelanin-based sexual pigmentation, prenesting body reserves, and condition at molt (reflected by growth bars and feather quality) vary across age classes. Melanin coverage correlated with condition at molt across age classes in males and showed high repeatability in both sexes. In contrast, carotenoid saturation increased longitudinally with age in males and correlated with condition at molt in different age classes in the 2 sexes. Specifically, carotenoid saturation correlated positively with condition at molt in younger, but not older males, whereas in females, the situation was reversed, with a positive correlation present only in older females. Results suggest that age-dependent signaling may promote maintenance of multifaceted sexual displays and that agedependent signaling dynamics depend on sex. © The Author 2013. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved

Declining extra-pair paternity with laying order associated with initial incubation behavior, but independent of final clutch size in the blue tit

Although functional explanations for female engagement in extra-pair copulation have been studied extensively in birds, little is known about how extra-pair paternity is linked to other fundamental aspects of avian reproduction. However, recent studies indicate that the occurrence of extra-pair offspring may generally decline with laying order, possibly because stimulation by eggs induces incubation, which may suppress female motivation to acquire extra-pair paternity. Here we tested whether experimental inhibition of incubation during the laying phase, induced by the temporary removal of eggs, resulted in increased extra-pair paternity, in concert with a later cessation of laying, in blue tits (Cyanistes caeruleus). As expected, experimental females showed a more gradual increase in nocturnal incubation duration over the laying phase and produced larger clutches than controls. Moreover, incubation duration on the night after the first egg was laid predicted how extra-pair paternity declined with laying order, with less incubation being associated with more extra-pair offspring among the earliest eggs in the clutch. However, incubation duration on this first night was unrelated to our experimental treatment and independent of final clutch size. Consequently, the observed decline in extra-pair paternity with laying order was unaffected by our manipulation and larger clutches included proportionally fewer extra-pair offspring. We suggest that female physiological state prior to laying, associated with incubation at the onset of laying, determines motivation to acquire extra-pair paternity independent of final clutch size. This decline in proportion of extra-pair offspring with clutch size may be a general pattern within bird species

Age before beauty? Relationships between fertilization success and age-dependent ornaments in barn swallows

When males become more ornamented and reproduce more successfully as they grow older, phenotypic correlations between ornament exaggeration and reproductive success can be confounded with age effects in cross-sectional studies, and thus say relatively little about sexual selection on these traits. This is exemplified here in a correlative study of male fertilization success in a large colony of American barn swallows (Hirundo rustica erythrogaster). Previous studies of this species have indicated that two sexually dimorphic traits, tail length and ventral plumage coloration, are positively correlated with male fertilization success, and a mechanism of sexual selection by female choice has been invoked. However, these studies did not control for potential age-related variation in trait expression. Here, we show that male fertilization success was positively correlated with male tail length but not with plumage coloration. We also show that 1-year-old males had shorter tails and lower fertilization success than older males. This age effect accounted for much of the covariance between tail length and fertilization success. Still, there was a positive relationship between tail length and fertilization success among older males. But as this group consisted of males from different age classes, an age effect may be hidden in this relationship as well. Our data also revealed a longitudinal increase in both tail length and fertilization success for individual males. We argue that age-dependent ornament expression and reproductive performance in males complicate inferences about female preferences and sexual selection