Who's your daddy? Paternity testing reveals promiscuity and multiple paternity in the carnivorous marsupial Dasyurus maculatus (Marsupialia: Dasyuridae)

Female promiscuity is common among mammals but its advantages, particularly for marsupials, remain unclear. Using microsatellite DNA from pouch young of known mothers, we identified the most likely fathers of 25 wild spotted-tailed quolls ( Dasyurus maculatus ) from six litters. We aimed to determine whether young within the same litter had different fathers, and whether breeding success of males was associated with large body mass (consistent with inter-male competition) or scrotal width (consistent with sperm competition). We also explored the possible influence of promiscuity on relatedness within litters. Finally, we used data on paternity and relatedness to make inferences regarding movement and dispersal.
Four litters were sired by more than one male, and three males sired offspring in more than one litter. Known fathers had higher body mass, but not scrotal width, than males of unknown paternity status, suggesting that males may compete for access to females. Sires were less related to dams than expected by chance, and litters with multiple paternity had lower relatedness than litters sired by a single male.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 1–7.     

Evidence for frequent incest in a cooperatively breeding mammal

As breeding between relatives often results in inbreeding depression, inbreeding avoidance is widespread in the animal kingdom. However, inbreeding avoidance may entail fitness costs. For example, dispersal away from relatives may reduce survival. How these conflicting selection pressures are resolved is challenging to investigate, but theoretical models predict that inbreeding should occur frequently in some systems. Despite this, few studies have found evidence of regular incest in mammals, even in social species where relatives are spatio-temporally clustered and opportunities for inbreeding frequently arise. We used genetic parentage assignments together with relatedness data to quantify inbreeding rates in a wild population of banded mongooses, a cooperatively breeding carnivore. We show that females regularly conceive to close relatives, including fathers and brothers. We suggest that the costs of inbreeding avoidance may sometimes outweigh the benefits, even in cooperatively breeding species where strong within-group incest avoidance is considered to be the norm.     

No evidence of sperm selection by female common shrews.

There is currently much interest in the suggestion that females are capable of post-copulatory (or cryptic) choice for male genetic compatibility. Here, I investigate this idea using data from mixed-paternity litters of the common shrew (Sorex araneus). Females of this species are highly promiscuous and, in natural populations, regularly incur costs of inbreeding by mating with close relatives. Selection should therefore favour female ability for sperm selection on the basis of male relatedness. No evidence was found in support of this idea. Relative number of offspring sired within mixed paternity litters was not significantly correlated with genetic similarity of males to the female mated. Relative fertilization success was, however, significantly related to male epididymal sperm counts. I conclude that most variation in relative fertilization success of male common shrews can be explained in terms of sperm competition, and that females of this species may not be capable of sperm selection.     

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.     

Effects of inbreeding on reproductive success,performance, litter size,and survival in captive red wolves (Canis rufus)

Captive‐breeding programs have been widely used in the conservation of imperiled species, but the effects of inbreeding, frequently expressed in traits related to fitness, are nearly unavoidable in small populations with few founders. Following its planned extirpation in the wild, the endangered red wolf (Canis rufus) was preserved in captivity with just 14 founders. In this study, we evaluated the captive red wolf population for relationships between inbreeding and reproductive performance and fitness. Over 30 years of managed breeding, the level of inbreeding in the captive population has increased, and litter size has declined. Inbreeding levels were lower in sire and dam wolves that reproduced than in those that did not reproduce. However, there was no difference in the inbreeding level of actual litters and predicted litters. Litter size was negatively affected by offspring and paternal levels of inbreeding, but the effect of inbreeding on offspring survival was restricted to a positive influence. There was no apparent relationship between inbreeding and method of rearing offspring. The observable effects of inbreeding in the captive red wolf population currently do not appear to be a limiting factor in the conservation of the red wolf population. Additional studies exploring the extent of the effects of inbreeding will be required as inbreeding levels increase in the captive population. Zoo Biol 29:36–49, 2010. © 2009 Wiley‐Liss, Inc.     

Seasonal change in the opportunity for sexual selection

Environmental and population parameters that influence the strength of sexual selection may vary considerably over the course of the reproductive season. However, the potential for sexual selection frequently fails to translate into variation in reproductive success among individuals. We investigated seasonal changes in variation in reproductive success, measured as the opportunity for sexual selection, using parentage analysis in 20 experimental populations of the European bitterling (Rhodeus amarus, Cyprinidae), a small freshwater fish with a promiscuous, resource-based mating system. We showed that although the largest males sired most offspring over the entire reproductive season, variation in reproductive success and hence the opportunity for sexual selection was low at the start of the season but increased significantly at its end. This seasonal difference probably arose from the superior competitive endurance of large males and from a higher temporal clustering of reproductively active females at the start of the breeding season than later in the season. The spatial distribution of oviposition sites had a negligible effect on the variation in reproductive success. We discuss the potential implications of our results for the importance and strength of sexual selection in natural populations.     

Mate choice, genetic incompatibility, and outbreeding in the ornate dragon lizard, Ctenophorus ornatus

There has been recent interest in the role genetic incompatibility may play in mate or sperm choice. One source of incompatibility may be too similar or disparate genomes. An isolated population of the ornate dragon lizard, Ctenophorus ornatus, was followed over a breeding season and parentage assigned to the offspring using microsatellites. It was found that the adults in the population had an eight per cent chance of mating with a relative. I examined whether C. ornatus mate (or fertilize their eggs) with respect to genetic similarity. There was no difference in a female's relatedness to the male in whose territory she resided and her average relatedness to all other males. Neither was there a difference in the relatedness of the male that sired a female's offspring and the female's average relatedness to all other males. There was no evidence of a cost to mating with a more genetically similar mate, because offspring survival was not influenced by degree of inbreeding or outbreeding. However, females that were more outbred had fewer offspring survive. In this small population there are two possible explanations for the decreased fitness associated with outbreeding. First, the species may have an evolutionary history of inbreeding and thus may be susceptible to outbreeding depression. Second. as fitter individuals produce more offspring, these offspring have an increased probability of breeding with relatives, leading to an indirect relationship between fitness and outbreeding.     

Consequences of a One-male Harem Reproductive System and Inbreeding in a Captive Group of <Emphasis Type="BoldItalic">Cercopithecus solatus</Emphasis>

In closed captive populations, where dispersal is not possible, kin recognition and behavioral avoidance are the only mechanisms by which closely related individuals can avoid inbreeding. In the absence of avoidance, a loss of genetic diversity is inevitable in successive generations.In the 1980s, the CIRMF in Gabon established a small breeding group of sun-tailed monkeys (Cercopithecus solatus) with 4 individuals, and subsequently 17 births have been registered. We aimed to describe via microsatellite genotyping the reproductive system in the colony of Cercopithecus solatus, to evaluate the loss of genetic diversity with succeeding generations, and to evaluate consequences of inbreeding depression on a measure of the lifespan reproductive success of females giving birth to inbred vs. noninbred offspring. During the 11-yr period for which data are available, only alpha males sired offspring, confirming a one-male social organization. They reproduced only during their period of tenure. Two of the 3 alpha males were responsible for all the infants born. Genetic diversity decreased and inbreeding coefficients increased with successive generations. Interbirth interval was increased following the birth of an inbred infant, indicating possible increased maternal costs of rearing inbred infants. Loss of genetic variability in this captive group of sun-tailed monkeys has led to significant inbreeding depression and demonstrates the importance of male-mediated gene flow in restricted one-male harem breeding groups.     

Inbreeding Depression and Inbreeding Avoidance in a Natural Population of Guppies (Poecilia reticulata)

Maintenance of genetic variation in the face of strong natural selection is a long‐standing problem in evolutionary biology. One of the most extreme examples of within‐population variation is the polymorphic, genetically determined color pattern of male Trinidad guppies (Poecilia reticulata). Female mating preference for rare or novel patterns has been implicated as a factor in maintaining this variation. The origin of this preference is not understood, although inbreeding avoidance has been proposed as a mechanism. Inbreeding avoidance is advantageous when populations exhibit inbreeding depression and the opportunity for mating between relatives exists. To determine whether these conditions are met in a natural guppy population, we assessed mating and reproductive patterns using polymorphic molecular markers. Females produced more offspring with less‐related males than with more‐related ones. In addition, females were more likely to have mated with less‐related males, but this trend was only marginally significant. Male heterozygosity was positively correlated with mating success and with the number of offspring sired, consistent with strong inbreeding depression for adult male fitness. These results provide substantial insight into mating patterns of a wild guppy population: strong inbreeding depression occurs, and individuals tend to avoid mating with relatives.     

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

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

Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Resolving the conundrum of inbreeding depression but no inbreeding avoidance: Estimating sex‐specific selection on inbreeding by song sparrows (Melospiza melodia)

Inbreeding avoidance among interacting females and males is not always observed despite inbreeding depression in offspring fitness, creating an apparent “inbreeding paradox.” This paradox could be resolved if selection against inbreeding was in fact weak, despite inbreeding depression. However, the net magnitude and direction of selection on the degree to which females and males inbreed by pairing with relatives has not been explicitly estimated. We used long‐term pedigree data to estimate phenotypic selection gradients on the degree of inbreeding that female and male song sparrows (Melospiza melodia) expressed by forming socially persistent breeding pairs with relatives. Fitness was measured as the total numbers of offspring and grand offspring contributed to the population, and as corresponding expected numbers of identical‐by‐descent allele copies, thereby accounting for variation in offspring survival, reproduction, and relatedness associated with variation in parental inbreeding. Estimated selection gradients on the degree to which individuals paired with relatives were weakly positive in females, but negative in males that formed at least one socially persistent pairing. However, males that paired had higher mean fitness than males that remained socially unpaired. These analyses suggest that net selection against inbreeding may be weak in both sexes despite strong inbreeding depression, thereby resolving the “inbreeding paradox.”     

Reproductive success by large, closely related males facilitated by sperm storage in an aggregate breeding amphibian

The outcome of sexual selection on males may depend on female mate choice and male–male competition as well as postcopulatory processes such as cryptic female choice and sperm competition. We studied the outcome of sexual selection in the spotted salamander ( Ambystoma maculatum ), specifically examining the role of body size and relatedness on male reproductive success. Using controlled mating experiments in the field, we gave females access to three males of different sizes. We used seven microsatellite loci to determine paternity in the resulting larvae, estimate relatedness ( r ) between females and their mates, and calculate md ² (a measure of within-individual genomic divergence), heterozygosity, and standardized heterozygosity in the larvae. Both body size and relatedness to the female were significant predictors of male reproductive success. The relatedness of the males available to a female did not influence the amount of stored sperm she used to sire her larvae. Nonetheless, computer simulations showed that the average md ², heterozygosity, and standardized heterozygosity of the offspring were lower than expected by random mating. These differences are due to the use of stored sperm to fertilize some eggs; md ², heterozygosity, and standardized heterozygosity of larvae sired by stored sperm were significantly lower than those of larvae sired by the experimental males. These results suggest that relatedness may further influence a male's long-term reproductive success by determining whether his sperm is stored for later breeding seasons. Sexual selection in this salamander likely involves a complex interaction among many factors and may act over many seasons.     

Re‐mating across years and intralineage polygyny are associated with greater than expected levels of inbreeding in wild red deer

The interaction between philopatry and nonrandom mating has important consequences for the genetic structure of populations, influencing co‐ancestry within social groups but also inbreeding. Here, using genetic paternity data, we describe mating patterns in a wild population of red deer (Cervus elaphus) which are associated with marked consequences for co‐ancestry and inbreeding in the population. Around a fifth of females mate with a male with whom they have mated previously, and further, females frequently mate with a male with whom a female relative has also mated (intralineage polygyny). Both of these phenomena occur more than expected under random mating. Using simulations, we demonstrate that temporal and spatial factors, as well as skew in male breeding success, are important in promoting both re‐mating behaviours and intralineage polygyny. However, the information modelled was not sufficient to explain the extent to which these behaviours occurred. We show that re‐mating and intralineage polygyny are associated with increased pairwise relatedness in the population and a rise in average inbreeding coefficients. In particular, the latter resulted from a correlation between male relatedness and rutting location, with related males being more likely to rut in proximity to one another. These patterns, alongside their consequences for the genetic structure of the population, have rarely been documented in wild polygynous mammals, yet they have important implications for our understanding of genetic structure, inbreeding avoidance and dispersal in such systems.     

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.     

Paternity success and the direction of sexual selection in a field population of a semelparous marsupial,Antechinus agilis

Antechinus agilis is a small sexually size dimorphic marsupial with a brief annual mating period of 2-3 weeks. All males die after this period, and females give birth to up to 10 young. Mating is thought to be promiscuous, however, there is no field data to confirm this. Using microsatellites, we investigated paternity patterns over two seasons in a wild population. Male weight was significantly positively related to the number of females fertilized and with the number of offspring sired, in both years. Furthermore, selection gradients indicated selection for larger males. Both results suggest that size dimorphism in A. agilis can be explained by sexual selection for larger males. The proportion of offspring sired within litters, did not relate to male size. Therefore, larger males are more successful through higher mating access, not through their sperm outcompeting that of smaller males. As expected from their known ranging behaviour, the number of offspring within litters left unassigned to a father did not depend on the grid location of the mother. Female size did not differ between successful reproducing and unsuccessful females. However, females that weaned offspring had larger heads than females that did not wean offspring. Males did not 'prefer' mating with larger females, nor did assortative mating occur. From our results, the mating system of A. agilis is clearly promiscuous. Selection for larger males occurred in both years, even though in one year the operational sex ratio was highly female biased, suggesting that the potential reproductive rate is a better predictor of the direction of sexual selection in A. agilis.     

Reproductive success in relation to dominance rank in the absence of prime-age males in Barbary macaques

In some primate species dominance rank of males is correlated with reproductive success, whereas in other species this relationship is inconsistent. Barbary macaques (Macaca sylvanus) live in a promiscuous mating system in which males are ranked in a dominance hierarchy that influences their access to females. High-ranking males usually monopolize fertile females during their estrous period and show increased mating activities. Subadult males generally rank below adult males. For Barbary macaque females in the Gibraltar colony, there was no correlation between dominance status and reproductive success. Paternity data for 31 offspring collected over four consecutive breeding seasons were used to test whether male social rank was associated with reproductive success and whether reproductive success was mainly confined to a small number of males. Genetic variation was assessed using 14 microsatellite markers for a dataset of 127 individuals sampled in all five social groups of the Gibraltar colony. Paternity analysis was conducted for offspring in one social group only, where all in-group males were sampled. Eighty-three percent of the offspring could be assigned to an in-group candidate father; none of the extra-group males appeared to have sired an infant. Male dominance rank was not found to contribute to the observed variation in male reproductive output. Fifty-nine percent of the offspring was sired by two low-ranking males, whereas the two top-ranking males sired one-fifth. A highly significant correlation was found for male age and dominance rank. Reproductive success of subadult males might be explained by the gap in the age distribution of male group members. These missing prime males are usually regarded as serious competitors for older males. Subadult males may have gained easier access to females in their absence. In addition, the presence of inbreeding avoidance mechanisms, which might also have overpowered possible rank effects, cannot be excluded.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

Behavioural inbreeding avoidance in wild African elephants

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.     

Extrapair mating between relatives in the barn swallow: a role for kin selection?

Why do females of many species mate with more than one male? One of the main hypotheses suggests that female promiscuity is an insurance mechanism against the potential detrimental effects of inbreeding. Accordingly, females should preferably mate with less related males in multiple or extrapair mating. Here we analyse paternity, relatedness among mating partners, and relatedness between parents and offspring, in the socially monogamous North American barn swallow (Hirundo rustica erythrogaster). In contrast to the inbreeding avoidance hypothesis, we found that extrapair mating partners were more related than expected by random choice, and tended to be more related than social partners. Furthermore, extrapair mating resulted in genetic parents being more related to their extrapair young than to their withinpair young. We propose a new hypothesis for extrapair mating based on kin selection theory as a possible explanation to these findings.