Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.     

Multiple paternities increase genetic diversity of offspring in Brandt's voles

Mating system and philopatry influence the genetic structure of a social group in mammals. Brandt's vole (Lasiopodomys brandtii) lives in social groups year-round and has male biased dispersal, which makes the vole a model system for studies of genetic consequences of mating system and philopatry. This study aimed to test the hypotheses that: (1) multiple paternity (MP) would exist in Brandt's voles, enhance offspring genetic diversity and reduce genetic relatedness between littermates; (2) promiscuity would occur in this species in that males and females mate with multiple partners; and (3) plural breeders of a social group would be genetically related because of philopatry of female juveniles in Brandt's voles. Paternity analysis indicated that MP occurred in 11 (46%) of 24 social groups examined and that promiscuity existed in this species. Multiple paternity litters had twice the offspring genetic diversity and half the average within-litter genetic relatedness of single paternity litters. We also found plural breeding females in six social groups. Average pairwise genetic relatedness of plural breeders ranged from 0.41 to 0.72 in four social groups, suggesting first-order kinship. Future studies need to investigate effects of reproductive skew and MP on population genetic structure of Brandt's voles.     

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet     

Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds

Studies aimed at determining why female birds often produce offspring sired by males other than their social mates generally compare traits of social and genetic mates. Here I examine paternity patterns in nests of the same female red-winged blackbirds (Agelaius phoeniceus) in successive breeding seasons. Returning females preferentially selected their former social mates as their new social mates when those males were present. However, paternity patterns were much less consistent. A female''s behaviour (faithful versus unfaithful) in one year did not predict her behaviour the following year. Females unfaithful in successive years did not prefer the same extra-pair males. Females unfaithful in one year that switched social mates the next year did not preferentially choose their former extra-pair mates as their new social mates. By switching genetic mates, females did not generally improve the quality of their mates. These results, together with previous analyses, suggest that female blackbirds in this population have little control over extra-pair mating. Although females may benefit from extra-pair mating because extra-pair males are generally longer lived, paternity patterns in this population are not consistent with extra-pair mating being part of a finely tuned female reproductive strategy.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata

We analysed the polygynous mating system of the bat Saccopteryx bilineata using behaviour observations and genetic data on 11 microsatellite DNA loci. Basic social units in S. bilineata are harem groups that consist of single males and up to eight females. Colonies comprise several harem groups, and the composition of colonies and harems is often stable over several reproductive seasons. The combination of parentage exclusion and likelihood-based parentage assignment in this study produced detailed parentage information for a large colony of S. bilineata. Reproduction occurred mostly within the colony (17% extra-colony paternity), but social associations in harems within the colony did not represent reproductive units (70% extra-harem paternity). The latter finding was consistent over three reproductive seasons. Spatial association of the roosting sites of males and females could not explain parentage patterns in the colony. Even though intra-harem paternity was less frequent than expected, it contributed significantly to reproduction of harem males. On average, the number of offspring sired by a male with females in his harem territory increased significantly with harem size, which corresponds to the higher energetic investment that is related to the maintenance of large harems. However, extra-harem paternity was not correlated with a male's harem size or intra-harem reproductive success. This suggests that individual preferences of females rather than male traits associated with the ability to defend large harems are most likely to cause the detected differences between social association and genetic mating system.     

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.     

Polyandry in coal tits Parus ater: fitness consequences of putting eggs into multiple genetic baskets

Females of many species mate with multiple males within a single reproductive cycle. One hypothesis to explain polyandry postulates that females benefit from increasing within-brood genetic diversity. Two mechanisms may render sire genetic diversity beneficial for females, genetic bet-hedging vs. non-bet-hedging. We analysed whether females of the socially monogamous coal tit (Parus ater) benefit via either of these mechanisms when engaging in extra-pair (i.e. polyandrous) mating. To obtain a measure of within-brood genetic diversity as a function of paternal genetic contributions, we calculated a sire diversity index based on the established Shannon-Wiener Index. In 246 broods from two consecutive years, sire genetic diversity had no effect on either the mean or the variance in brood fitness measured as offspring recruitment within 4 years after birth. The hypothesis that benefits of increasing sire diversity contribute to selection for female extra-pair mating behaviour in P. ater was therefore not supported.     

Turtle mating patterns buffer against disruptive effects of climate change

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.     

Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax)

We studied patterns of genetic relatedness and paternity in moustached tamarins, small Neotropical primates living in groups of 1–4 adult males and 1–4 adult females. Generally only one female per group breeds, mating with more than one male. Twin birth are the norm. In order to examine the genetic consequences of this mating pattern, DNA was extracted from fecal samples collected from two principal and six neighboring groups. DNA was characterized at twelve microsatellite loci (average: seven alleles/locus). We addressed the following questions: Do all adult males have mating access to the reproductive female of the group? How is paternity distributed across males in a group? Can polyandrous mating lead to multiple paternity? Are nonparental animals more closely related to the breeders than to the population mean? And, are mating partners unrelated? Breeding females mated with all nonrelated males. In at least one group the father of the older offspring did not sire the youngest infant although he was still resident in the group. We also found evidence for multiple paternity in a supposed twin pair. Yet, within each group the majority (67–100%) of infants had the same father, suggesting reproductive skew. Relatedness within groups was generally high (average R = 0.31), although both nonrelated males and females occurred, i.e., immigrations of both sexes are possible. Mating partners were never found to be related, hence inbreeding seems to be uncommon. The results suggest that while the social mating system is polyandry, paternity is often monopolized by a single male per group. Am J Phys Anthropol, 2005. © 2004 Wiley-Liss, Inc.     

Female aggression predicts mode of paternity acquisition in a social lizard

Individual differences in behaviour are ubiquitous in nature. Despite the likely role of selection in maintaining these differences, there are few demonstrations of their fitness consequences in wild populations and, consequently, the mechanisms that link behavioural variation to variation in fitness are poorly understood. Specifically, the consequences of consistent individual differences in behaviour for the evolution of social and mating strategies have rarely been considered. We examined the functional links between variation in female aggression and her social and mating strategies in a wild population of the social lizard Egernia whitii. We show that female Egernia exhibit temporally consistent aggressive phenotypes, which are unrelated to body size, territory size or social density. A female''s aggressive phenotype, however, has strong links to her mode of paternity acquisition (within- versus extra-pair paternity), with more aggressive females having more offspring sired by extra-pair males than less aggressive females. We discuss the potential mechanisms by which female aggression could underpin mating strategies, such as the pursuit/acceptance of extra-pair copulations. We propose that a deeper understanding of the evolution and maintenance of social and mating systems may result from an explicit focus on individual-level female behavioural phenotypes and their relationship with key reproductive strategies.     

Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm

In social Hymenoptera (ants, bees, and wasps), the number of males that mate with the same queen affects social and genetic organization of the colony. However, the selective forces leading to single mating in certain conditions and multiple mating in others remain enigmatic. In this study, I investigated whether queens of the wood ant Formica paralugubris adopting different dispersal strategies varied in their mating frequency (the number of males with whom they mated). The frequency of multiple mating was determined by using microsatellite markers to genotype the sperm stored in the spermatheca of queens, and the validity of this method was confirmed by analysing mother–offspring combinations obtained from experimental single-queen colonies. Dispersing queens, which may found new colonies, did not mate with more males than queens that stayed within polygynous colonies, where the presence of numerous reproductive individuals ensured a high level of genetic diversity. Hence, this study provides no support to the hypotheses that multiple mating is beneficial because it increases genetic variability within colonies. Most of the F. paralugubris queens mated with a single male, whatever their dispersal strategy and life history. Moreover, multiple mating had little effect on colony genetic structure: the effective mating frequency was 1.11 when calculated from within-brood relatedness, and 1.13 when calculated from the number of mates detected in the sperm. Hence, occasional multiple mating by F. paralugubris queens may have no adaptive significance.     

Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.     

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.     

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.     

Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry

The proximate mechanisms underlying the evolution and maintenance of within-sex variation in mating behaviour are still poorly understood. Species characterized by alternative reproductive tactics provide ideal opportunities to investigate such mechanisms. Bluegill (Lepomis macrochirus) are noteworthy in this regard because they exhibit two distinct cuckolder (parasitic) morphs (called sneaker and satellite) in addition to the parental males that court females. Here we confirm previous findings that spawning cuckolder and parental males have significantly different levels of testosterone and 11-ketotestosterone. We also report, for the first time, that oestradiol and cortisol levels are higher in cuckolders than in parental males. The two cuckolder morphs did not differ in average levels of any of the four hormones. However, among satellite males which mimic females in appearance and behaviour, there was a strong negative relationship between oestradiol levels and body length, a surrogate for age. This finding suggests that for satellite males, oestradiol dependency of mating behaviour decreases with increasing mating experience. Although such decreased hormone dependence of mating behaviour has been reported in other taxa, our data represent the first suggestion of the relationship in fishes.     

The measure and significance of Bateman's principles

Bateman''s principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman''s principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman''s principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman''s principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.     

Female and Male Moths Display Different Reproductive Behavior when Facing New versus Previous Mates

Multiple mating allows females to obtain material (more sperm and nutrient) and/or genetic benefits. The genetic benefit models require sperm from different males to fertilize eggs competitively or the offspring be fathered by multiple males. To maximize genetic benefits from multiple mating, females have evolved strategies to prefer novel versus previous mates in their subsequent matings. However, the reproductive behavior during mate encounter, mate choice and egg laying in relation to discrimination and preference between sexes has been largely neglected. In the present study, we used novel and previous mate treatments and studied male and female behavior and reproductive output in Spodoptera litura. The results of this study do not support the sperm and nutrient replenishment hypotheses because neither the number of mates nor the number of copulations achieved by females significantly increased female fecundity, fertility and longevity. However, females showed different oviposition patterns when facing new versus previous mates by slowing down oviposition, which allows the last male has opportunities to fertilize her eggs and the female to promote offspring diversity. Moreover, females that have novel males present called earlier and more than females that have their previous mates present, whereas no significant differences were found on male courtship between treatments. These results suggest that S. litura females can distinguish novel from previous mates and prefer the former, whereas males generally remate regardless of whether the female is a previous mate or not. In S. litura, eggs are laid in large clusters and offspring competition, inbreeding and disease transfer risks are thus increased. Therefore, offspring diversity should be valuable for S. litura, and genetic benefits should be the main force behind the evolution of female behavioral strategies found in the present study.