Male age and its association with reproductive traits in captive and wild house sparrows

Evolutionary theory predicts that females seek extra‐pair fertilizations from high‐quality males. In socially monogamous bird species, it is often old males that are most successful in extra‐pair fertilizations. Adaptive models of female extra‐pair mate choice suggest that old males may produce offspring of higher genetic quality than young males because they have proven their survivability. However, old males are also more likely to show signs of reproductive senescence, such as reduced sperm quality. To better understand why old males account for a disproportionally large number of extra‐pair offspring and what the consequences of mating with old males are, we compared several sperm traits of both captive and wild house sparrows, Passer domesticus. Sperm morphological traits and cloacal protuberance volume (a proxy for sperm load) of old and young males did not differ substantially. However, old males delivered almost three times more sperm to the female's egg than young males. We discuss the possibility of a post‐copulatory advantage for old over young males and the consequences for females mated with old males.     

Extra‐pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine

Despite considerable research effort, it remains unclear whether extra‐pair fertilizations (EPF) drive the evolution of male secondary ornamentation in socially monogamous systems. In this study, we test the hypothesis that EPF contribute to the evolution or maintenance of male feather ornamentation in a sexually dichromatic passerine, the Scarlet Rosefinch, Carpodacus erythrinus. We show that the colouration of ornamental breast feathers is a good predictor of basic sources of variation in male annual reproductive output in rosefinches and that the annual realized reproductive success of males is positively associated with measures of ornamental colouration only when gains and losses because of EPF are considered. The results indicate that EPF in rosefinches may rely on absolute (good genes) rather than self referential (genetic complementarity) criteria of mate choice. Our study corroborates the potentially important role of EPF in the evolution and/or maintenance of elaborate male ornaments in socially monogamous taxa.     

Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design

Extra-pair copulations (EPC) are the rule rather than an exception in socially monogamous birds, but despite widespread occurrences, the benefits of female infidelity remain elusive. Most attention has been paid to the possibility that females gain genetic benefits from EPC, and fitness comparisons between maternal half-siblings are considered to be a defining test of this hypothesis. Recently, it was shown that these comparisons may be confounded by within-brood maternal effects where one such effect may be the distribution of half-siblings in the laying order. However, this possibility is difficult to study as it would be necessary to detect the egg from which each chick hatched. In this study, we used a new approach for egg-chick assignment and cross-fostered eggs on an individual basis among a set of nests of the collared flycatcher Ficedula albicollis. After hatching, chicks were ascribed to mothers and therefore to individual eggs by molecular genetic methods. Extra-pair young predominated early in the laying order. Under natural conditions, this should give them a competitive advantage over their half-siblings, mediated by hatching asynchrony. However, we experimentally synchronized hatching, and after this treatment, extra-pair young did not outperform within-pair young in any studied trait including survival up to recruitment and several indicators of reproductive success and attractiveness. We obtained only modest sample sizes for the last two traits and did not test for extra-pair success of male offspring. Thus, we cannot exclude the possibility of advantages of extra-pair young during the adult phase of life. However, our data tentatively suggest that the more likely reason for females' EPCs is the insurance against the infertility of a social mate.     

Variation in social organization influences the opportunity for sexual selection in a social lizard

Social monogamy has traditionally been suggested to be maintained because of weak sexual selection on male partner acquisition. However, the ubiquitous incidence of extra-pair paternity suggests that sexual selection can be strong in monogamous systems, although studies partitioning variance in male reproductive success have come to mixed conclusions. Here, we use detailed field data to examine variance in male reproductive success and its implications for the maintenance of sociality in a population of the socially monogamous lizard Egernia whitii. We show that both within-pair and, to a lesser extent, extra-pair partner acquisition contribute to the variance in male reproductive success, resulting in considerable opportunity for sexual selection. Despite this, levels of multiple mating are lower in Egernia compared to other reptiles, suggesting that male partner acquisition is constrained. We suggest that this constraint may be a result of strong territoriality combined with sexual conflict over multiple mating generated by costs of extra-pair paternity to females as a result of facultative male care. This has the potential to limit sexual selection by reducing variance in male reproductive success and therefore contribute to the maintenance of complex social organization.     

Sperm morphology and sperm velocity in passerine birds

Sperm velocity is one of the main determinants of the outcome of sperm competition. Since sperm vary considerably in their morphology between and within species, it seems likely that sperm morphology is associated with sperm velocity. Theory predicts that sperm velocity may be increased by enlarged midpiece (energetic component) or flagellum length (kinetic component), or by particular ratios between sperm components, such as between flagellum length and head size. However, such associations have rarely been found in empirical studies. In a comparative framework in passerine birds, we tested these theoretical predictions both across a wide range of species and within a single family, the New World blackbirds (Icteridae). In both study groups, sperm velocity was influenced by sperm morphology in the predicted direction. Consistent with theoretical models, these results show that selection on sperm morphology and velocity are likely to be concomitant evolutionary forces.     

Polyandry and postcopulatory sexual selection in a wild population

When females mate multiply, postcopulatory sexual selection can occur via sperm competition and cryptic female choice. Although postcopulatory selection has the potential to be a major force in driving evolution, few studies have estimated its strength in natural populations. Likewise, although polyandry is widespread across taxa and is the focus of a growing body of research, estimates of natural female mating rates are still limited in number. Microsatellites can be used to estimate the number of mates represented in females' sperm stores and the number of sires contributing to their offspring, enabling comparisons both of polyandry and of two components of postcopulatory selection: the proportion of males that mate but fail to sire offspring, and the degree of paternity skew among the males that do sire offspring. Here, we estimate the number of mates and sires among wild females in the Hawaiian swordtail cricket Laupala cerasina. We compare these estimates to the actual mating rates and paternity shares we observed in a semi‐natural population. Our results show that postcopulatory sexual selection operates strongly in this species: wild females mated with an average minimum of 3.6 males but used the sperm from only 58% of them. Furthermore, among the males that did sire offspring, paternity was significantly skewed. These patterns were similar to those observed in the field enclosure, where females mated with an average of 5.7 males and used the sperm from 62% of their mates, with paternity significantly skewed among the sires.     

Sexually selected nest-building--Pomatoschistus minutus males build smaller nest-openings in the presence of sneaker males

Both natural selection and sexual selection may act on nest-building. We tested experimentally how different regimes of egg-predation and male-male competition influence nest-building before mating, using the marine fish sand goby, Pomatoschistus minutus. Males with sneaker males present built the smallest nest-openings, smaller than males held alone or with Pomatoschistus microps males (which may predate eggs and compete over nest-sites but not compete over fertilizations). Males with visual access to other nest-building males tended also to build smaller openings than males held alone or with P. microps. Males with egg-predators present built nests with openings not differing significantly from any other treatment. Our results indicate that the small nest-openings found in the sneaker male treatment are sexually selected through protection against sneaking or by female choice. Across treatments, time span before a male started to build his nest also explained variation in nest-opening width; males starting late built larger nest-openings.     

Multiple genetic benefits of female promiscuity in a socially monogamous passerine

The adaptive function of female extrapair mating in socially monogamous passerines is currently debated. In the bluethroat (Luscinia s. svecica), a previous study showed that offspring sired by extrapair males had a higher cell-mediated immunity than their within-pair half siblings, suggesting an immunogenetic benefit of extrapair mating in this species. Here, we expanded that dataset with two more years and investigated the association between extrapair paternity and microsatellite multilocus heterozygosity, in addition to cell-mediated immunity. We found that extrapair offspring were more heterozygous than their within-pair half siblings, and corroborated the previous finding of enhanced cellular immunity in extrapair offspring in this four-year dataset. The increased heterozygosity among extrapair offspring appeared to be a result of extrapair mates being less genetically similar than pair mates, and also less genetically similar than expected by random choice. Together with previous findings in this species, showing that the majority of females participate in extrapair copulations, our results indicate a postcopulatory cryptic female choice of genetically dissimilar males. The enhanced cellular immunity and increased heterozygosity were not related to each other, and hence our results indicate two independent genetic benefits of extrapair mating in the bluethroat.     

Evidence of genetic monogamy in the lemur Indri (Indri indri)

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.     

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird

Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality‐related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density‐dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.     

The ecological-evolutionary interplay: density-dependent sexual selection in a migratory songbird

Little is understood about how environmental heterogeneity influences the spatial dynamics of sexual selection. Within human-dominated systems, habitat modification creates environmental heterogeneity that could influence the adaptive value of individual phenotypes. Here, we used the gray catbird to examine if the ecological conditions experienced in the suburban matrix (SM) and embedded suburban parks (SP) influence reproductive strategies and the strength of sexual selection. Our results show that these habitats varied in a key ecological factor, breeding density. Moreover, this ecological factor was closely tied to reproductive strategies such that local breeding density predicted the probability that a nest would contain extra-pair offspring. Partitioning reproductive variance showed that while within-pair success was more important in both habitats, extra-pair success increased the opportunity for sexual selection by 39% at higher breeding densities. Body size was a strong predictor of relative reproductive success and was under directional selection in both habitats. Importantly, our results show that the strength of sexual selection did not differ among habitats at the landscape scale but rather that fine-scale variation in an ecological factor, breeding density, influenced sexual selection on male phenotypes. Here, we document density-dependent sexual selection in a migratory bird and hypothesize that coarse-scale environmental heterogeneity, in this case generated by anthropogenic habitat modification, changed the fine-scale ecological conditions that drove the spatial dynamics of sexual selection.     

Extra‐Pair Paternity Declines with Female Age and Wing Length in the Pied Flycatcher

Despite many studies of how male characteristics affect paternity in predominantly monogamous birds, relatively little attention has been given to the traits of females that may influence extra‐pair paternity (EPP). However, the occurrence of EPP may be the result of behavioural interactions in which both male and female traits are important for determining the outcome. If EPP is driven mainly by female choice of extra‐pair sires, older, more experienced or larger females would be better able to evade mate guarding tactics and more capable of selecting extra‐pair mates and resisting unwanted suitors. This would be especially noticeable in females paired with unattractive mates. On the other hand, if EPP is driven mainly by male pursuit, we should expect that young, inexperienced or small females would be more exposed to coercive male approaches independently of social mate traits. In a study of an Iberian population of the pied flycatcher Ficedula hypoleuca, we found that EPP affected 38% of the broods and 17% of the nestlings. These values are relatively high, allowing a relatively large number of affected within‐pair mates to be included. We found that EPP is related to both female and male traits although not to any interaction between male and female traits. EPP was higher at nests tended by both younger and short‐winged females and by browner males. Older females may be more experienced and dominant while long‐winged females may be faster fliers, these traits enabling them to avoid extra‐pair copulations, while brown males are less aggressive towards male intruders. In our study population, EPP appears to be caused by male pursuit, which in some cases may overwhelm female attempts to avoid extra‐pair copulations and their social partner's ability to prevent them.     

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.     

Extra‐pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean

Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen‐mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra‐pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed brood paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra‐pair males in a nonrandom, self‐matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a compatible genes model for extra‐pair mate choice where the optimal allelic diversity is intermediate, not maximal. This golden mean presumably reflects a trade‐off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra‐pair mating is adaptive through altered genetic constitution in offspring.     

Extra pair paternity in birds: a review of interspecific variation and adaptive function

The application of molecular genetic techniques has revolutionized our view of avian mating systems. Contrary to prior expectations, birds are only very rarely sexually monogamous, with 'extra-pair offspring' found in approximately 90% of species. Even among socially monogamous species, over 11% of offspring are, on average, the result of extra-pair paternity (EPP). Based on over 150 molecular genetic studies of EPP in birds, we review two topical areas: (i) ecological explanations for interspecific variation in the rate of EPP; and (ii) evidence bearing on the adaptive function of EPP. We highlight the remaining challenges of understanding the relative roles of genes and ecology in determining variation between taxa in the rate of extra paternity, and testing for differences between extra-pair offspring and those sired within-pair.     

Development of microsatellite markers for parentage analysis in the great tinamou (Tinamus major)

Eighteen microsatellite loci were isolated from great tinamous (Tinamus major), which are large terrestrial birds found in the Neotropics. These are the first primers developed for the Order Tinamiformes. Paternity analyses are possible because the levels of heterozygosity are sufficiently high (0.29-0.90).     

No evidence of sperm conjugate formation in an Australian mouse bearing sperm with three hooks

Sperm conjugation occurs when two or more sperm physically unite for motility or transport through the female reproductive tract. In many muroid rodent species, sperm conjugates have been shown to form by a single, conspicuous apical hook located on the sperm head. These sperm “trains” have been reported to be highly variable in size and, despite all the heads pointing in roughly the same direction, exhibit a relatively disordered arrangement. In some species, sperm “trains” have been shown to enhance sperm swimming speed, and thus have been suggested to be advantageous in sperm competition. Here, we assessed the behavior of sperm in the sandy inland mouse (Pseudomys hermannsburgensis), a muroid rodent that bears sperm with three apical hooks. First, we accrued genetic evidence of multiple paternity within “wild” litters to unequivocally show that sperm competition does occur in this species. Following this we utilized both in vitro and in vivo methodologies to determine whether sandy inland mouse sperm conjugate to form motile trains. Our observations of in vitro preparations of active sperm revealed that sandy inland mouse sperm exhibit rapid, progressive motility as individual cells only. Similarly, histological sections of the reproductive tracts of mated females revealed no in vivo evidence of sperm conjugate formation. We conclude that the unique, three‐hooked morphology of the sandy inland mouse sperm does not facilitate the formation of motile conjugates, and discuss our findings in relation to the different hypotheses for the evolution of the muroid rodent hook/s.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.