Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.)

The primary objective of this study was to use highly polymorphic microsatellite loci to estimate individual reproductive success in Atlantic salmon based on the number of surviving juveniles (young of the year) at the population level under natural conditions. We inferred reproductive strategies adopted by both sexes by applying a maximum likelihood method to determine parent-offspring genotype relationships. A high degree of variance in individual reproductive success for both males and females was revealed. The high number of mates used by both sexes is not concordant with previous behavioral studies proposing that females are mainly monogamous in this species. We found little evidence supporting the prediction from previous reports of a positive relationship between individual size and realized reproductive success for either males or females. For both sexes, however, there was a significant correlation between the number of mates and the number of offspring. These results indicate that this species' mating system is more flexible than previously thought and suggest that factors such as potential genetic benefits or environmental uncertainty may also be driving the evolution and the plasticity of mating systems in Atlantic salmon.     

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

Understanding the mating system and reproductive success of a species provides evidence for sexual selection. We examined the mating system and the reproductive success of captive adult black sea bream (Acanthopagrus schlegelii), using parentage assignment based on two microsatellites multiplex PCR systems, with 91.5% accuracy in a mixed family (29 sires, 25 dams, and 200 offspring). Based on the parentage result, we found that 93.1% of males and 100% of females participated in reproduction. A total of 79% of males and 92% of females mated with multiple partners (only 1 sire and 1 dam were monogamous), indicating that polygynandry best described the genetic mating system of black sea bream. For males, maximizing the reproductive success by multiple mating was accorded with the sexual selection theory while the material benefits hypothesis may contribute to explain the multiple mating for females. For both sexes, there was a significant correlation between mating success and reproductive success and the variance in reproductive success of males was higher than females. Variation in mating success is the greatest determinant to variation in reproductive success when the relationship is strongly positive. The opportunity for sexual selection of males was twice that of females, as well as the higher slope of the Bateman curve in males suggested that the intensity of intrasexual selection of males was higher than females. Thus, male–male competition would lead to the greater variation of mating success for males, which caused greater variation in reproductive success in males. The effective population number of breeders (N_b) was 33, and the N_b/N ratio was 0.61, slightly higher than the general ratio in polygynandrous fish populations which possibly because most individuals mated and had offspring with a low variance. The relatively high N_b contributes to the maintenance of genetic diversity in farmed black sea bream populations.     

Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae)

The short- and long-term consequences of monogamy and promiscuity in an aphidophagous ladybird, Propylea dissecta (Mulsant) in terms of reproductive performance and offspring fitness were investigated. Promiscuous females were more fecund and laid more viable eggs than monogamous ones. Amongst promiscuous females, those mated with multiple males (freedom for mate choice) had significantly higher reproductive output than those mated daily with a new unmated male. The increased reproductive output of females mated with an unmated male each day in comparison to monogamous ones might possibly be a result of their increased ejaculate size. The further increase in reproductive output, when a female was allowed to choose a mate, may be because of repeated preferential mating with the fitter males. Results on long-term consequences of promiscuity revealed faster development and increased survival in offspring of promiscuous females at 25, 27 and 30 degrees C. The percent adult emergence was more strongly influenced than development by the mating regime. There were no statistically significant differences in survival of offspring of promiscuous females (mate choice) at the three temperatures, while the percent survival of offspring of monogamous females differed significantly. Offspring of promiscuous females (mate choice) were fittest in terms of development and survival, which indicates their probable better genetic constitution and subsequently that of chosen mates. Thus, promiscuity has both short- and long-term benefits and is advantageous to ladybirds. The presence of long-term benefits in terms of fitter offspring probably indicates the evolutionary rationale behind the prevalence of promiscuity in ladybirds.     

Male reproductive success and sexual selection in northern water snakes determined by microsatellite DNA analysis

Male northern water snakes (Nerodia sipedon) have high variancein reproductive success relative to females. We used DNA-basedpaternity analyses from a 3-year study of two marsh populationsof water snakes to investigate the factors that contributeto variation in male success. Male traits investigated includedbody size, condition, tail length, home range size, activityduring the mating season, and genetic profile (genetic similarityto females, heterozygosity, and genetic variability [d²]).We successfully assigned > 80% of offspring to sires froma sample of 811 offspring from 45 litters. Male reproductivesuccess did not vary significantly with body size, tail length,condition, home range size, or the number of microsatelliteloci at which males were heterozygous, nor with other featuresof their genetic profiles. However, we found evidence of positive assortative mating by size in the marsh in which receptive femaleswere not spatially clumped. Also, males that were most activeduring the mating season were more successful, particularlywhere females were not clumped. We failed to find evidenceof selection acting on male size through variance in reproductivesuccess, indicating that sexual selection does not have an important influence on sexual size dimorphism in this species(males are smaller than females). We propose that males aresmaller than females because the lack of advantage to largesize allows males to adopt a low-energy, low-growth strategythat reduces their risk of predation outside the mating season.     

Division of labor in the monogamous goby,Valenciennea longipinnis, in relation to burrowing behavior

Feeding and burrowing behavior of the monogamous gobiid fish,Valenciennea longipinnis, were studied on the coral reef at Sesoko Island, Okinawa, Japan. These fish usually live in pairs, the male and female feeding in close proximity to one another upon benthic animals and constructing several burrows cooperatively for purposes of shelter or spawning. Paired females fed more and burrowed less frequently than their mates. Because burrow maintenance was mostly conducted by the latter, the paired females performed work much less frequently than solitary females. Thus, the paired females may be able to allocate more energy toward egg production. The division of labor related to burrowing behavior in this species may be an effective way to increase reproductive success for both sexes. Moreover, the fameles burrowed even less frequently when paired with larger males, probably because burrowing ability may be correlated with mouth size in males. This is a likely reason for the preference of females to mate with larger males.     

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.     

The sex lives of parasites: Investigating the mating system and mechanisms of sexual selection of the human pathogen Schistosoma mansoni

The mating systems of internal parasites are inherently difficult to investigate although they have important implications for the evolutionary biology of the species, disease epidemiology, and are important considerations for control measures. Using parentage analyses, three topics concerning the mating biology of Schistosoma mansoni were investigated: the number of mates per adult male and female, variance in reproductive success among individuals, and the potential role for sexual selection on male body size and also mate choice for genetically dissimilar individuals. Results indicated that schistosomes were mostly monogamous, and evidence of only one mate change occurred over a period of 5-6 weeks. One male was polygynous and contained two females in its gynecophoral canal although offspring were only detected for one of the females. Even though they were primarily monogamous and the sex ratio near even, reproductive success was highly variable, indicating a potential role for sexual selection. Male body size was positively related to reproductive success, consistent with sexual selection via male-male competition and female choice for large males. However, relatedness of pairs was not associated with their reproductive success. Finally, genetically identical individuals differed significantly in their reproductive output and identical males in their body size, indicating important partner and environmental effects on these traits.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.     

The sexy son hypothesis: data from the pied flycatcher Ficedula hypoleuca

The sexy son hypothesis has been proposed as a possible explanation for polygyny in territorial birds. Females mated with polygynous males are assumed to derive benefits in future generations through their ‘sexy’ sons, and hence they can afford to produce fewer offspring than simultaneously breeding monogamous females, the polygyny threshold thus being reduced. In the pied flycatcher, secondary females are not fully aided by males in feeding the nestlings, and they produce only 65% as many fledglings as do simultaneous monogamous and primary females. We have proposed male deception through polyterritoriality as the explanation for females ending up as secondary females, while some authors have advocated the sexy son hypothesis as an alternative. However, secondary females do not achieve benefits in future generations in this species. Repeatability of male mating status is far too low to grant any significant benefits through grandsons. In fact, offspring hatched in secondary female nests suffer from food shortage and therefore are of poor phenotypic quality with low fledging weight and short tarsus length. Therefore they are likely to enjoy lower reproductive success than offspring born in monogamous nests, as is illustrated by data on the relation between lifetime reproductive success and tarsus length. Altogether the applicability of the sexy son hypothesis is limited since it is based on the unrealistic assumption of relatively high heritability for a character with great influence on male fitness.     

Drosophila melanogaster females change mating behaviour and offspring production based on social context

In Drosophila melanogaster, biological rhythms, aggression and mating are modulated by group size and composition. However, the fitness significance of this group effect is unknown. By varying the composition of groups of males and females, we show that social context affects reproductive behaviour and offspring genetic diversity. Firstly, females mating with males from the same strain in the presence of males from a different strain are infecund, analogous to the Bruce effect in rodents, suggesting a social context-dependent inbreeding avoidance mechanism. Secondly, females mate more frequently in groups composed of males from more than one strain; this mitigates last male sperm precedence and increases offspring genetic diversity. However, smell-impaired Orco mutant females do not increase mating frequency according to group composition; this indicates that social context-dependent changes in reproductive behaviour depend on female olfaction, rather than direct male-male interactions. Further, variation in mating frequency in wild-type strains depends on females and not males. The data show that group composition can affect variance in the reproductive success of its members, and that females play a central role in this process. Social environment can thus influence the evolutionary process.     

The effects of the minimum threshold condition for breeding on offspring sex-ratio adjustment in the lesser kestrel

We propose a model for sex-ratio adjustment complementary to that of Trivers and Willard. In addition to the three basic assumptions of the Trivers-Willard model, our model assumes that the sex with more variable reproductive success (normally male) is also the sex less constrained for reproduction. This assumption seems realistic, because several studies have demonstrated that poor-condition males may adopt alternative mating strategies and sire some offspring, whereas females have physiological constraints for gestation or egg production that cannot be avoided. Thus, under these circumstances, sons of both poor and good condition would be more valuable for parents than daughters, whereas daughters would be relatively more valuable than sons at intermediate condition. This model predicts, therefore, a U-shaped relationship between parental condition and offspring sex ratio. We present a case study for the monogamous lesser kestrel (Falco naumanni) that fulfills the assumptions and predictions of the model. The minimum body condition for breeding, measured as pectoral thickness, was lower for sons than for daughters. Below this minimum, males had a higher chance of breeding than females. Above this minimum, however, the lifetime reproductive success was condition dependent in males but not in females. Thus, males in better body condition attain, on average, higher reproductive success than females. Offspring sex ratio varied with the size of the father's ornaments and mother condition according to the U-shaped pattern predicted by the model.     

Social mating system and reproductive success in house wrens

Current models explaining the establishment and maintenanceof social monogamy and polygyny within avian populations typicallyassume that the reproductive success of polygynous males exceedsthat of monogamous males. This assumption is almost always supportedwhen the number of fledglings or recruits to future breedingpopulations is used to measure adult reproductive success. However,recent studies using DNA markers indicate that simple countsof fledglings or recruits may be a poor estimator of the numberof nestlings sired by the social father. In this paper, we comparethe number of genetic offspring produced by socially monogamousand polygynous house wren (TrogiodyUs atdon) males in nestsat which they were the social father. Polygynous males did,in fact, sire more nestlings in their own nests than did monogamousmales. Moreover, although we have not identified the sires ofextrapair nestlings, we document that even when all extrapairnestlings in this population are hypotheticaOy assigned to monogamousmales, die total reproductive success of polygynous males exceedsthat of monogamous males. These results and those of severalother recent studies are consistent with the assumption thatpolygynous males produce more offspring than monogamous males.     

Females Remate for Sperm Replenishment in a Seed Bug: Evidence from Offspring Viability

Females of many insects mate multiply but why they do so remains controversial. Here we investigated the effects of multiple matings on female reproductive success of a New Zealand seed bug, Nysius huttoni. We found little evidence for females to gain material (nutritional) benefits through multiple matings because the number of matings did not have significant effect on female fecundity. Females remated to the same males or different males produced similar number of viable offspring, suggesting that females do not obtain genetic benefit from remating in terms of offspring viability. With the increase of the number of matings, however, overall fertility rate significantly increased and daily fertility rate declined significantly slower over time. These results suggest that females remate for the replenishment of sperm. Five matings are sufficient for females to maximize their reproductive success, and additional matings appear to be superfluous. However, the females of this bug mate as many as 68 times if males and females are paired for lifetime. This can be explained by the convenience hypothesis, i.e., females remate superfluously to minimize the costs of harassment by promiscuous males.     

Genotype and extra-pair paternity in the house wren: a rare-male effect?

Females in socially monogamous species may select extra-pair (EP) mates to increase the heterozygosity, and hence fitness, of their offspring. We tested this hypothesis in the house wren (Troglodytes aedon), a largely monogamous songbird in which EP young are common. We typed paired males and females, nestlings, and males on neighbouring territories, at five to seven microsatellite loci over 2 years in a Wyoming, USA, population. We identified EP sires at 20 nests with EP young. In pairwise comparisons, we found no significant differences between cuckolded within-pair (WP) males and EP sires in three measures of heterozygosity (mean d2, standardized heterozygosity and internal relatedness). However, EP sires had fewer alleles that were common within the population than did the WP males they cuckolded. Nearby males who were EP sires also had fewer common alleles than did nearby males who did not sire EP young. Females in our population may be more prone to accept copulations from males with rare genotypes than from males with common genotypes. Alternatively, selection of rare-male sperm may occur within the female reproductive tract. Because mating with rare males is likely to increase offspring heterozygosity, our data suggest that EP mating may provide genetic benefits to females.     

Female survival,lifetime reproductive success and mating status in a passerine bird

In facultatively polygynous birds, secondary females of polygynously mated males typically have reduced annual reproductive success, because polygynous males provide less paternal care than monogamous males. Life history theory predicts that, as a result of increased reproductive investment, secondary females should suffer from reduced survival and lifetime reproductive success, but previous studies provided only weak support for this hypothesis. We used 7 years of data to study the fitness of female collared flycatchers Ficedula albicollis in relation to mating status by estimating survival and lifetime reproductive success. Taking differences in recapture probability into account, a mark-recapture analysis revealed that females observed at least once to breed as secondary female had higher survival than other females. This relationship was not confounded by laying date, because when we assessed the impact of laying date on survival, we found similar survival patterns. Females of polygynous males had reduced breeding success in terms of number of young fledged during the current reproductive event. However, during their lifetime females found at least once in primary or secondary mating status produced significantly more eggs, and at least the same number of fledglings and recruits as monogamous females. Thus, in the collared flycatcher, females of polygynously mated males seem to suffer from mating status during the most recent reproductive event, but considering survival and lifetime reproductive success, the apparently disadvantageous mating event is not necessarily associated with reduced residual reproductive value.     

Mating system and reproductive skew in the black rhinoceros

Only approximately 2600 black rhinoceros survive today, mainly in small, isolated populations of < 100 animals. The management of remaining black rhinoceros populations aims at preserving natural levels of genetic relatedness and optimizing breeding success, which requires an accurate knowledge of the mating system, reproductive skew and effective population size. DNA was extracted from faecal samples from a community of 35 wild black rhinoceros, and microsatellites were used to characterize patterns of paternity of 19 offspring born from eight females in this community. Paternity could be ascribed unequivocally for each offspring. Although our conclusions must be considered tentative, we present the first genetic evidence that black rhinoceros males are polygynous, with a high variance in reproductive success. We also describe a noninvasive management tool that can be used for the genetic management of this critically endangered species, both in the wild and in captivity.     

Extra‐pair offspring are less heterozygous than within‐pair offspring in American redstarts Setophaga ruticilla

The vast majority of bird species are socially monogamous; however, extra‐pair paternity is nearly ubiquitous and a number of theories have been proposed to explain the prevalence of this mixed mating strategy. Here, we test the genetic compatibility hypothesis – the idea that females seek extra‐pair copulations with males whose genes are more compatible with her own. For this study, we examined eight years of paternity data (2004–2011) from a Nearctic‐Neotropical migratory bird, the American redstart Setophaga ruticilla, breeding in southeastern Ontario, Canada. We predicted that females paired with genetically similar males (higher relatedness) would be more likely to produce extra‐pair offspring and that extra‐pair offspring would have higher levels of heterozygosity than within‐pair offspring. Alternatively, because this population experiences high levels of immigration, females may produce extra‐pair offspring with more genetically similar males because of the potential for outbreeding depression. Using five highly variable microsatellite markers, we examined patterns of relatedness among social pairs as well as measures of offspring heterozygosity. In contrast to our predictions, we found no difference in relatedness between social pairs where the females produced extra‐pair offspring and social pairs where the females produced only within‐pair offspring. However, extra‐pair offspring were significantly less heterozygous than within‐pair offspring. Together, these findings suggest that females a) are not engaging in extra‐pair fertilizations based on relatedness to their social mate and b) appear to be mating with extra‐pair males that are more genetically similar to themselves. We suggest there may be benefits for females to mate with genetically similar extra‐pair males in highly outbred populations with high rates of immigration, such as for maintaining co‐adapted gene complexes or genes coding for local adaptations.