Social Mates Research Articles

Rock sparrow song reflects male age and reproductive success.

The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.

Extrapair copulations reduce inbreeding for female red-backed fairy-wrens, Malurus melanocephalus

In many socially monogamous species, females copulate with and produce offspring sired by males other than their social mates, yet it remains controversial whether or how females benefit from these ‘extrapair’ copulations. Recently, it has been suggested that females might benefit if they are able to copulate with extrapair males that are genetically dissimilar to themselves, thereby potentially increasing the heterozygosity and/or reducing the level of inbreeding of the resulting offspring. However, empirical tests of this hypothesis have been criticized because a low number of molecular markers can lead to biased estimates of relatedness among individuals, and because all studies to date have been correlational and therefore unable to rule out potentially confounding factors. The red-backed fairy-wren is a bird with very limited dispersal, and hence the risks of inbreeding are high. We used a panel of microsatellite markers to examine paternity and relatedness between mates in this species, and also conducted an experiment that manipulated relatedness between a female and her social mate. Results from both approaches showed that females paired to genetically similar males were more likely to produce young sired by extrapair males, and that those offspring were less inbred (more heterozygous) than within-pair offspring. Thus, female fairy-wrens are able to avoid the potential costs of close inbreeding through extrapair copulations.

Alternative matings and the opportunity costs of paternal care in house sparrows

Among avian species with biparental care, male alternative reproductive opportunities can occur in the form of either extrapair fertilizations or additional social mates. We manipulated testosterone (T) levels in male house sparrows to assess whether participation in parental care detracts from male success in securing alternative matings; we also compared the annual reproductive success of males that engaged in normal levels of care with the success of males that displayed increased mating effort at the expense of parental care. Our results showed that the incidence of polygyny among high-T/low-parenting males was elevated relative to control males, but that success in obtaining extrapair mates was independent of hormonal treatment. Thus, male parental care seems to carry an opportunity cost in terms of reduced acquisition of additional social mates. Despite this cost, between-treatment comparisons of the estimated number of fledglings sired annually suggest that, in this species, the value of male contributions to care is sufficiently high to favor the reductions in T that facilitate normal male parenting.

Female mate choice based on territory quality in barn swallows

Female mate choice based on territory quality is difficult to study because territories often contain many resources, which are difficult to quantify. Here, using the barn swallow (Hirundo rustica gutturalis) breeding at an outdoor breeding site in Japan, where each male defends only a small territory containing old nests, we studied whether females choose social mates based on territory quality. Since the territories of this species contain few other resources, territory quality can easily be assessed by quantifying old nests in the territory. We made the following four observations: (1) male swallows displayed old nests in their territories to females; (2) the old nests used for the first clutch were less broken than the other old nests within the same territory; (3) territory quality, defined by the number of old nests weighted by the intactness of each old nest, predicted the productivity of the territory; and (4) males with better territories paired with females earlier, and hence bred earlier, than those with inferior territories. The relationships remained significant even after controlling for male morphological traits. Based on these results, we can infer that female swallows choose their mates based, in part, on territory quality.

Heterozygosity and fitness benefits of extrapair mate choice in White-rumped Swallows (Tachycineta leucorrhoa)

Female birds that engage in extrapair mating may choose extrapair mates that are genetically compatible, increasing their fitness through genetic benefits, such as increased heterozygosity, to their offspring; or choose mates that are heterozygous at one or more loci. Here, we describe the extrapair mating system, explore the fitness benefits of extrapair mating and test the heterozygosity hypothesis in White-rumped Swallows (Tachycineta leucorrhoa) breeding in Argentina using a panel of microsatellite loci. Extrapair offspring accounted for 56% of the nestlings and 77% of the broods in our population. Within broods, 1–4 males fathered extrapair offspring, and in 29% of nests, all offspring were from extrapair sires. We found that broods with extrapair offspring fledged overall more young than broods with no extrapair offspring but that the young that died were more heterozygous than the ones that fledged. Although extrapair offspring had a higher probability of surviving than within-pair offspring, these 2 groups did not differ in their level of heterozygosity. Neither the heterozygosity of the social mate nor the genetic similarity of the social pair predicted the presence of extrapair young. Instead, females chose social mates that were significantly less genetically similar to them. Our results do not support the heterozygosity hypothesis and contradict 2 of its main predictions.

Inclusive fitness of ‘kissing cousins’: new evidence of a role for kin selection in the evolution of extra-pair mating in birds

Social monogamy is nearly ubiquitous across avian taxa,but evidence from a proliferation of studies utilizing molecular paternity analysis suggests that sexual monogamy is the rare exception rather than the rule (Griffith et al. 2002). Efforts to explain the prevalence of extra-pair paternity (EPP) have largely focused on the potential fitness benefits for offspring genetic quality, as females are less likely to benefit directly from seeking extra-pair mates. In particular, there has been considerable interest in the degree to which EPP may represent an adaptive female strategy to avoid inbreeding (or outbreeding)depression when paired with a highly related (or unrelated)social mate (Kempenaers 2007). Others have argued that, because relatives share many genes identical by descent,females might increase their own inclusive fitness by providing additional breeding opportunities to genetically related males (Waser et al. 1986; Kokko & Ots 2006). Thus, in the absence of significant inbreeding depression, pursuing EPP with relatives should be favoured by kin selection, although there exist few unambiguous empirical examples of such preferences in the literature. In this issue of Molecular Ecology, Wang &Lu (2011) present an analysis of mating patterns with respect to genetic relatedness of social and extra-pair partners in the ground tit (Parus humilis), a facultative cooperative breeder in which socially monogamous pairs occasionally form cooperative groups with unpaired helper males (Fig. 1). Consistent with the predictions of the kin-selection hypothesis, females in both bi-parental and cooperative groups preferentially engaged in extra-pair matings with relatives, irrespective of relatedness to their social mates, and while suffering no apparent costs of inbreeding depression in their progeny. These finding shave several exciting implications for our understanding of avian mating system diversity and the evolution of cooperative breeding.

Estimating genetic benefits of polyandry from experimental studies: a meta‐analysis

The consequences of polyandry for female fitness are controversial. Sexual conflict studies and a meta-analysis of mating rates in insects suggest that there is a longevity cost when females mate repeatedly. Even so, compensatory material benefits can elevate egg production and fertility, partly because polyandry ensures an adequate sperm supply. Polyandry can therefore confer direct benefits. The main controversy surrounds genetic benefits. The argument is analogous to that surrounding the evolution of conventional female mate choice, except that with polyandry it is post-copulatory mechanisms that might bias paternity towards males with higher breeding values for fitness. Recent meta-analyses of extra-pair copulations in birds have cast doubt on whether detectable genetic benefits exist. By contrast, another meta-analysis showed that polyandry elevates egg hatching success (possibly due to a fertilization bias towards sperm with paternal genes that elevate embryo survival) in insects. A detailed summary of whether polyandry elevates other components of offspring performance is lacking. Here we present a comprehensive meta-analysis of 232 effect sizes from 46 experimental studies. These experiments were specifically designed to try to quantify the potential genetic benefits of polyandry by controlling fully for the number of matings by females assigned to monandry and polyandry treatments. The bias-corrected 95% confidence intervals for egg hatching success (d = -0.01 to 0.61), clutch production (d = 0.07 to 0.45) and fertility (d = 0.04 to 0.40) all suggest that polyandry has a beneficial effect (although P values from parametric tests were marginally non-significant at P = 0.075, 0.052 and 0.058, respectively). Polyandry was not significantly beneficial for any single offspring performance trait (e.g. growth rate, survival, adult size), but the test power was low due to small sample sizes (suggesting that many more studies are still needed). We then calculated a composite effect size that provides an index of general offspring performance. Depending on the model assumptions, the mean effect of polyandry was either significantly positive or marginally non-significant. A possible role for publication bias is discussed. The magnitude of the reported potential genetic benefits (d = 0.07 to 0.19) are larger than those from two recent meta-analyses comparing offspring sired by social and extra-pair mates in birds (d = 0.02 to 0.04). This difference raises the intriguing possibility that cryptic, post-copulatory female choice might be more likely to generate 'good gene' or 'compatible gene' benefits than female choice of mates based on the expression of secondary sexual traits.

Female ground tits prefer relatives as extra-pair partners: driven by kin-selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.

Additive Genetic Variance, Heritability, and Inbreeding Depression in Male Extra-Pair Reproductive Success

The hypothesis that female extra-pair reproduction in socially monogamous animals reflects indirect genetic benefits requires that there be additive and/or nonadditive genetic variance in fitness. However, the specific hypotheses that male extra-pair reproductive success (EPRS) shows additive genetic variance (V(A)), heritability (h2), or inbreeding depression, and hence that females could acquire indirect genetic benefits through increased EPRS of sons, have not been explicitly tested. We used comprehensive genetic pedigree data from song sparrows (Melospiza melodia) to estimate V(A), h2, and inbreeding depression in the number of extra-pair offspring a male sired per year and the probability that a male would sire any extra-pair offspring per year. Inbreeding depression was substantial: more inbred males sired fewer extra-pair offspring and were less likely to sire any extra-pair offspring. In contrast, estimates of V(A) and h2 were close to 0, although 95% credible intervals were relatively wide. These data suggest that females could accrue indirect genetic benefits, in terms of increased EPRS of outbred sons, by mating with unrelated social or extra-pair mates. In contrast, any indirect benefit of extra-pair reproduction in terms of producing sons with high additive genetic value for EPRS is most likely to be small.

Causes of lifetime fitness of Darwin's finches in a fluctuating environment

The genetic basis of variation in fitness of many organisms has been studied in the laboratory, but relatively little is known of fitness variation in natural environments or its causes. Lifetime fitness (recruitment) may be determined solely by producing many offspring, modified by stochastic effects on their subsequent survival up to the point of breeding, or by an additional contribution made by the high quality of the offspring owing to nonrandom mate choice. To investigate the determinants of lifetime fitness, we measured offspring production, longevity, and lifetime number of mates in four cohorts of two long-lived species of socially monogamous Darwin's finch species, Geospiza fortis and G. scandens, on the equatorial Galápagos Island of Daphne Major. Regression analysis showed that the lifetime production of fledglings was predicted by lifetime number of clutches and that recruitment was predicted by lifetime number of fledglings and longevity. There was little support for a hypothesis of selective mating by females. The offspring sired by extrapair mates were no more fit in terms of recruitment than were half-sibs sired by social mates. These findings provide insight into the evolution of life history strategies of tropical birds. Darwin's finches deviate from the standard tropical pattern of a slow pace of life by combining tropical (long lifespan) and temperate (large clutch size) characteristics. Our study of fitness shows why this is so in terms of selective pressures (fledgling production and adult longevity) and ecological opportunities (pulsed food supply and relatively low predation).

Plumage color and food availability affect male reproductive success in a socially monogamous bird

Male reproductive success in socially monogamous birds is influenced to varying degrees by within-pair fertilization (WPF) and extrapair fertilization (EPF). In many species, males of higher phenotypic quality (e.g., plumage color) are more likely to obtain EPFs; however, predictors of WPF success have been less consistently identified. Moreover, few studies have examined the influence of ecological variables on patterns of paternity, even though environmental conditions are known to affect mating behavior of male and female birds. In this study, we examined phenotypic and ecological factors influencing patterns of paternity in broods of mountain bluebirds, Sialia currucoides. We show that brighter, bluer males were more likely to obtain EPFs in first broods but that plumage color did not predict the ability of males to maintain paternity in their own nest. We then examined the effect of food availability in first broods on the probability of males losing paternity in second broods within the same season. Females that were provided with supplemental food throughout first breeding attempts were less likely to produce extrapair offspring in second broods, and we suggest that supplemented females may have been less likely to seek extrapair mating opportunities because they perceived their social mates to be of higher quality under conditions of enhanced food availability. Our results demonstrate that ecological variables such as food availability can influence patterns of paternity and suggest that consideration of environmental context will be important for future research investigating mate choice and sexual selection in socially monogamous species. Key words: extrapair paternity, food availability, mountain bluebird, plumage color. [Behav Ecol]

Female Cape sugarbirds (Promerops cafer) modify egg investment both for extra‐pair mates and for male tail length

The differential allocation hypothesis predicts that females should invest more in reproduction when paired with attractive males. We measured egg volume in Cape sugarbirds (Promerops cafer), a sexually dimorphic passerine, in relation to paternity of the offspring and in response to an experimental tail length treatment. We manipulated tail length, after pair formation, but before egg laying: males had their tails either shortened or left unmanipulated. Our manipulation was designed to affect female allocation in a particular breeding attempt rather than long-term mate choice: males with shortened tails would appear to be signalling at a lower level than they should given their quality. We found that egg volume was smaller in the nests of males with experimentally shortened tails but larger when the offspring were the result of extra-pair matings. Both these findings are consistent with the differential allocation hypothesis. We suggest that tail length may be used by females as a cue for mate quality, eliciting reduced female investment when breeding with social mates; and with males with shortened tails.

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra-pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.

Paternal Song Complexity Predicts Offspring Sex Ratios Close to Fledging, but not Hatching, in Song Sparrows

Abstract Sex allocation theory predicts that population sex ratios should be generally stable and close to unity, but individuals may benefit by adjusting the sex ratio of their offspring. For example, females paired with attractive males may benefit by overproducing sons relative to daughters, as sons inherit their fathers' attractive ornaments (“sexy son” hypothesis). Similarly, if compatible gene effects on fitness are more pronounced in males than females, genetically dissimilar mated pairs may enhance fitness by overproducing sons (“outbred son” hypothesis). We tested these hypotheses in Song Sparrows (Melospiza melodia) by examining offspring sex ratios of 64 complete families shortly after hatching (“early-stage”) and again shortly before fledging (“late-stage”) in relation to paternal song complexity and the genetic similarity of social mates. Neither early nor late-stage offspring sex ratio was related to parental genetic similarity. Nests of males with larger song repertoires contained more male...

Male Red-winged Blackbirds with experimentally dulled epaulets experience no disadvantage in sexual selection

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Extra-pair paternity in waved albatrosses: genetic relationships among females, social mates and genetic sires

Summary Interactions among close relatives are expected to be common in colonially breeding species, species with limited geographic distributions such as island endemics, or those with limited natal or breeding dispersal. The waved albatross, Phoebastria irrorata, a colonially nesting, endemic seabird in Galapagos, Ecuador, presents an opportunity to closely examine relationships between genetic similarity of parents and extra-pair paternity. This species’ mating system is characterized by high year-to-year social mate and nest site fidelity as well as an unexpectedly high level of extra-pair paternity. The probability of hatching was lower for social pairs with high genetic similarity, suggesting an apparent cost of inbreeding. Despite this apparent cost, analyses of multilocus minisatellite band-sharing coefficients revealed that genetic similarity was somewhat negatively associated with EPF probability, inconsistent with the pattern predicted by the Genetic Similarity Hypothesis (GSH) that social pairs with extrapair offspring would be more similar than those with within-pair offspring. We found that a model with no effect of the type of dyad the female was in (female–social mate compared to female–genetic sire) on genetic similarity was as heavily weighted as one incorporating an effect, also inconsistent with the GSH. Evidence from our analyses suggested that cuckolded males were more genetically similar to randomly drawn males than to the genetic sire of their extra-pair offspring, a finding in contrast to the main prediction of our novel EPF tolerance hypothesis that males might tolerate extra-pair offspring if the actual sire is closely related. We discuss these findings in light of information about dispersal and we present some alternative explanations for extra-pair paternity in the waved albatross.

Hatching order explains an extrapair chick advantage in western bluebirds

Within-family comparisons of offspring growth rates have provided important tests of genetic benefits of extrapair mating for females. Here, we demonstrate that hatching order explains the growth advantage for extrapair young in western bluebirds (Sialia mexicana); extrapair nestlings are larger than within-pair nestlings in the same nest, but they also hatch earlier in the clutch, thus benefiting from hatching asynchrony. By controlling for hatch order and other nongenetic factors and comparing mixed-paternity broods with genetically monogamous broods, we show that the extrapair nestling growth advantage is not genetically based. We cannot rule out the possibility that females benefit from extrapair mating because genetic quality indicators may appear later in life and may be independent of hatch order, however, based on our results, we do not see evidence of genetic superiority of extrapair nestlings. Although findings similar to ours have been attributed to maternal effects, it is currently unclear whether overrepresentation of extrapair nestlings early in the laying and hatching sequence results from investment patterns of females, their social mates, or extrapair males. This study highlights the need to investigate the potentially complex interactions among all players, and how these may lead to higher performance of extrapair offspring compared with within-pair offspring within the same family.

Long tails matter in sugarbirds—positively for extrapair but negatively for within-pair fertilization success

Extrapair mating is known to occur in many animals and potentially has a significant influence on reproductive success. Female extrapair mate choice may explain the occurrence of exaggerated ornaments in socially monogamous species, but the influence of ornamentation on extrapair mating success has rarely been investigated experimentally. Cape sugarbirds (Promerops cafer) are socially monogamous, almost always lay 2 egg clutches and have long-term pair bonds often lasting several seasons. However, they also display sexually dimorphic extravagant ornamentation in the form of a long, graduated tail and have one of the highest rates (65% of young) of extrapair paternity recorded in birds. We provide a test of the hypothesis that the ornamented tail is used in mate choice for extrapair partners by conducting an experiment in which tail length was manipulated after social mating but before copulation. This experiment therefore allowed females to respond to the manipulation of male tail length when making a choice of copulation partner but not social mate. We show that the tail length of male sugarbirds has a significant effect on the success of males in gaining extrapair paternity, with long-tailed males obtaining significantly more extrapair young than shorttailed males. However, males with short tails sire a significantly greater proportion of the nestlings in their own nests than longtailed individuals. This result suggests that males may adopt alternative strategies dependent on their ornamentation. Key words: extrapair mating, mate choice, Pomerops cafer, sexual selection, sugarbird, tail ornamentation. [Behav Ecol]

Female Barn Swallows Gain Indirect but not Direct Benefits through Social Mate Choice

AbstractFemale mate choice is responsible for the evolution of male secondary sexual ornaments. If male ornamental traits reflect indirect, genetic benefits and/or direct, material benefits to females, choosy females may benefit from their choice, indirectly and/or directly. We examined a breeding population of Japanese barn swallowsHirundo rustica gutturalisto determine whether male tail streamer length reflected indirect and/or direct benefits to females. There was no significant positive relationship between male streamer length and the number of extra‐pair young (EPY) sired, suggesting that male tail streamers are not a signal of indirect benefits (i.e. good genes theory). In addition, we found no evidence that males with longer streamers fed their offspring more frequently or sired more within‐pair young (WPY). The result indicates that male streamer length probably does not act as a signal of direct benefits. Our finding that the length of tail streamers in Japanese barn swallows plays no role in sexual selection is not consistent with studies on European subspecies, but is consistent with studies on North American subspecies where sexual selection on tail streamer is weak. The present study supports the recent suggestion that the pattern of sexual selection on tail streamer length in barn swallows varies geographically. Instead of tail length, males in better condition sired more EPY and WPY. Males in better condition, however, did not feed their nestling more frequently. These results indicate that females gain indirect benefits but not direct benefits, in terms of feeding of young, on choosing social mates.

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner's heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.