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.     

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Natal dispersal and parental escorting predict relatedness between mates in a passerine bird

Although relatedness between mates is of considerable evolutionary and ecological significance, the way in which the level of relatedness is determined by different behavioural processes remains largely unknown. We investigated the role of behaviour in predicting mate relatedness in great tits using genotypic markers and detailed observations. We studied how mate relatedness is influenced by natal dispersal, inbreeding/outbreeding avoidance after natal dispersal and a behaviour not previously considered that influences membership to social aggregations, namely family escorting behaviour by parents. Among locally born individuals, the level of mate relatedness decreased with natal dispersal distance for females, but not for males. In contrast, mate relatedness was negatively related to the extent of family movements for males, but not for females. However, family movements did not predict dispersal distance for either sex. Local recruits were more related to their mates than immigrants, but this was only significant for females. No evidence was found for inbreeding/outbreeding avoidance after dispersal. Our results suggest that, in highly mobile species, mating options are spatially and/or socially limited, and that parents influence mating options of their offspring before dispersal.     

Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix)

Although inbreeding depression and mechanisms for kin recognition have been described in natural bird populations, inbreeding avoidance through mate choice has rarely been reported suggesting that sex‐biased dispersal is the main mechanism reducing the risks of inbreeding. However, a full understanding of the effect of dispersal on the occurrence of inbred matings requires estimating the inbreeding risks prior to dispersal. Combining pairwise relatedness measures and kinship assignments, we investigated in black grouse whether the observed occurrence of inbred matings was explained by active kin discrimination or by female‐biased dispersal. In this large continuous population, copulations between close relatives were rare. As female mate choice was random for relatedness, females with more relatives in the local flock tended to mate with genetically more similar males. To quantify the initial risks of inbreeding, we measured the relatedness to the males of females captured in their parental flock and virtually translocated female hatchlings in their parental and to more distant flocks. These tests indicated that dispersal decreased the likelihood of mating with relatives and that philopatric females had higher inbreeding risks than the actual breeding females. As females do not discriminate against relatives, the few inbred matings were probably due to the variance in female dispersal propensity and dispersal distance. Our results support the view that kin discrimination mate choice is of little value if dispersal effectively reduces the risks of inbreeding.     

Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks

Mate selection for inbreeding avoidance is documented in several taxa. In mammals, most conclusive evidence comes from captive experiments that control for the availability of mates and for the level of genetic relatedness between mating partners. However, the importance of mate selection for inbreeding avoidance as a determinant of siring success in the wild has rarely been addressed. We followed the reproduction of a wild population of eastern chipmunks (Tamias striatus) during five breeding seasons between 2006 and 2009. Using molecular tools and parentage assignment methods, we found that multiple paternity (among polytocous litters) varied from 25% in an early-spring breeding season when less than a quarter of females in the population were reproductively active to 100% across three summer breeding seasons and one spring breeding season when more than 85% of females were reproductively active. Genetically related parents were common in this population and produced less heterozygous offspring. Furthermore, litters with multiple sires showed a higher average relatedness among partners than litters with only a single sire. In multiply sired litters, however, males that were more closely related to their partners sired fewer offspring. Our results corroborate findings from captive experiments and suggest that selection for inbreeding avoidance can be an important determinant of reproductive success in wild mammals.     

STORM: software for testing hypotheses of relatedness and mating patterns

Storm is a software package that allows users to test a variety of hypotheses regarding patterns of relatedness and patterns of mate choice and/or mate compatibility within a population. These functions are based on four main calculations that can be conducted either independently or in the hypothesis-testing framework: internal relatedness; homozygosity by loci; pairwise relatedness; and a new metric called allele inheritance, which calculates the proportion of loci at which an offspring inherits a paternal allele different from that inherited from its mother. STORM allows users to test four hypotheses based on these calculations and Monte Carlo simulations: (i) are individuals within observed associations or groupings more/less related than expected; (ii) do observed offspring have more/less genetic variability (based on internal relatedness or homozygosity by loci) than expected from the gene pool; (iii) are observed mating pairs more/less related than expected if mating is random with respect to relatedness; and (iv) do observed offspring inherit paternal alleles different from those inherited from the mother more/less often than expected based on Mendelian inheritance.     

High rates of infidelity in the Grey Fantail Rhipidura albiscapa suggest that testis size may be a better correlate of extra‐pair paternity than sexual dimorphism

The Grey Fantail Rhipidura albiscapa is a socially monogamous passerine endemic to Australia. Behavioural and morphological clues point to opposing conclusions as to its breeding system; sexual monomorphism and monochrome colorations suggest monogamy, whereas relatively large testes and a prominent cloacal protruberance are more indicative of multiple mating and sperm competition. We used five highly variable microsatellite loci to investigate the genetic breeding system of this species. Paternity was assigned to 49 of 69 (71%) offspring tested and the overall rate of partner infidelity was high, with 55% of offspring being sired by an extra‐pair male and 64% of all clutches containing extra‐pair young. This puts the Grey Fantail amongst the most promiscuous socially monogamous species yet studied. Where extra‐pair fathers were identified, these were invariably in neighbouring territories, and although larger males did not gain more paternities overall, extra‐pair offspring tended to be fathered by larger males than expected by chance. We interpret our findings in light of some of the potential costs and benefits associated with extra‐pair paternity.     

Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors

In chimpanzees (Pan troglodytes), high-ranking males are expected to have high reproductive success and females typically emigrate upon reaching maturity. Although high average relatedness among males in the same social groups has been assumed, previous reports have indicated that relatedness among males is not necessarily significantly higher than that among females. The paternity of 11 offspring and the relatedness of 50 individuals in the M group of chimpanzees at Mahale Mountains National Park, Tanzania, were investigated using DNA analyses. We determined the fathers of 10 offspring. Two different alpha males sired a total of five offspring, whereas the other males had low reproductive success. The proportion of paternal half-sibling pairs among the 10 offspring was 15.6%. The average relatedness among mature males was significantly higher than that among mature females. The existence of an old male and the long tenure of one alpha male may have contributed to this significant difference. The average dyadic relatedness among mature natal individuals was significantly higher than that in natal-immigrant pairs in which the individuals came from different groups. The average relatedness among immigrant females was similar to that in pairs of natal and immigrant females, suggesting that the immigrants came from various groups. Thus, female transfer acts to maintain low average relatedness within the group. A comparison of our results to those from other study sites suggests that although the average relatedness among adult males does not reach the level of half-siblings, under some circumstances it can exceed the relatedness of females.     

Patterns of paternal relatedness in British grey seal colonies

Previous studies of breeding behaviour in the grey seal, Halichoerus grypus, have painted conflicting pictures. Behavioural observations suggest a classical polygynous system with a small number of dominant males fathering most of the offspring. However, genetic analysis suggests that many potential fathers spend little time ashore, that some pairs of seals show partner fidelity and that the dominant males are not as successful as their behaviour would suggest. Here we used paternal relatedness between pups with known mothers, sampled over an 11-year period, to show that behavioural dominance leading to enhanced fitness is a feature of only a handful of males located near the centre of the breeding colony. The vast majority of pups are fathered by any of a large number of males who all share approximately equal success, including virtually all those males who have previously escaped our best sampling efforts. As expected, the frequency of full-sibs is reduced in this longer time series relative to the original study. However, absolute estimates of the frequency of full-sibs seem to be confounded by a tendency for females who produce paternally unrelated pups to have conceived to males who are more genetically dissimilar from each other than expected by chance alone. Together, these elements of breeding behaviour would help to maintain maximum genetic diversity and to minimize the effects of inbreeding.     

Parental genetic similarity and offspring performance in blue tits in relation to brood size manipulation

In birds, as in many other taxa, higher genetic similarity of mates has long been known to reduce offspring fitness. To date, the majority of avian studies have focused on examination whether the genetic similarity of social mates predicts hatching success. Yet, increased genetic similarity of mates may also reduce offspring fitness during later life stages, including the nestling period and beyond. Here, we investigated whether parental genetic similarity influences offspring performance using data from free‐living blue tits (Cyanistes caeruleus) collected across three breeding seasons. Additionally, we tested whether brood size manipulation affects the magnitude and direction of the relationship between genetic similarity of mates and offspring performance. Sixteen microsatellite markers were used to measure genetic similarity between biological parents. We found that the genetic similarity of parents negatively affects offspring immune response and this effect was independent of the experimental brood size manipulation.     

Isolation and characterization of new microsatellite markers from the Japanese flounder (Paralichthys olivaceus)

The isolation and characterization of eight polymorphic microsatellite loci from a Japanese flounder partial genomic library are reported. The eight markers isolated in this study were highly polymorphic and their positions on the linkage genome map of the Japanese flounder were determined. Therefore, they are useful for ecological studies of wild populations. These markers are more effective than other markers with no information of chromosomal locations.     

Individual phenotype, kinship, and the occurrence of inbreeding in song sparrows

Inbreeding load, a key parameter in evolutionary ecology, is frequently estimated by regressing fitness (or related traits) on inbreeding coefficient across population members. This approach assumes that inbreeding occurs randomly with respect to an individual's intrinsic ability to produce fit offspring; estimated loads might otherwise be biased by covariation between inbreeding and individual quality. This assumption, however, is rarely validated. We tested whether, in free-living song sparrows Melospiza melodia, an individual's observed kinship with its social mate (and hence the degree of inbreeding in which an individual participated) was correlated with specific phenotypic traits that are likely to indicate individual quality. Males (and to some extent females) that hatched earlier within their cohort, had shorter tarsi, bred earlier during their first year, or survived fewer years paired with more closely related mates and therefore produced relatively inbred offspring. These correlations arose because males with specific phenotypes were more closely related to the female population (and therefore more likely to pair with closer relatives under random pairing), and because males with specific phenotypes paired with closer relatives than expected. Such correlations could bias estimated inbreeding loads, and should be considered in quantitative genetic analyses of phenotypic variance in populations in which inbreeding occurs.     

Multiple paternity in a philopatric rodent: the interaction of competition and choice

Paternity confusion is often suggested as the benefit that femalemammals accrue by mating with multiple males, but genetic advantagesare also possible. Microsatellite-based parentage analyses demonstratethat female banner-tailed kangaroo rats (Dipodomys spectabilis)commonly mate with more than one male; we asked how male andfemale behaviors interact to influence the characteristics ofmales that sire offspring. Specifically, we compared attributes(age, weight, mobility, relatedness, proximity) of the fathersof 229 known-maternity offspring with those of the other malesaccessible to the mothers. Adult males living adjacent to eachfemale attempt to monopolize access to her, and the nearestmale sires a plurality of offspring, but most mothers' youngare fathered by more than one male and littermates are usuallyhalf-sibs. Male proximity and mobility, but not size, influencethe probability of paternity, suggesting a role for competitivemate searching. Females significantly reduce the inbreedingcoefficient of their offspring by mating with males other than(or in addition to) the nearest male. Fathers are less closelyrelated to the mother in years of high density when unrelatedmales are more accessible to the female. Our results favor thegenetic "bet-hedging" hypothesis, whereby females actively butunselectively seek matings with additional males when the malemost likely to win in mate competition is costly to her (inthis case, genetically less compatible). We anticipate thatgenetic bet hedging will be common in species whose femalesare defendable, especially if they are also philopatric.     

Isolation and characterization of microsatellite markers from the budgerigar,Melopsittacus undulatus

The budgerigar, Melopsittacus undulatus, belongs to a group of birds that are among the most common captive‐held avian species that are also most threatened. Budgies are also a valuable resource as model species for many important vertebrate characteristics including auditory and ageing. Several microsatellite‐enriched genomic libraries were developed using standard protocols. Twelve of 20 primer pairs developed from microsatellite‐containing sequences were codominant and polymorphic when tested on 21 birds from three different states. The number of alleles detected ranged from two to four, with the expected and observed heterozygosities ranging from 0.09 to 0.61 and from 0.00 to 0.85, respectively. The genomic libraries and the primers described here will be useful in characterizing budgies.     

The colour of paternity: extra‐pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs

In socially monogamous species, individuals can use extra‐pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra‐pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed‐morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra‐pair paternity, offspring sex ratio or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory.     

Extrapair fertilization and genetic similarity of social mates in the Mexican jay

Inbreeding depression should favor the ability of females toavoid inbreeding or minimize its effects. We tested for a relationshipbetween genetic similarity of social pairs and the occurrenceof extrapair fertilization (EPF) in the Mexican jay (Aphelocomaultramarina). Multilocus minisatellite and microsatellite DNAfingerprinting was used to detect extrapair young and measuregenetic similarity between social parents. We found that 12of 31 (39%) nests had at least one EPF and 15 of 93 (16%) youngwere the result of EPF. The mean DNA fingerprinting band sharingscore between social mates who had at least one EPF was significantlyhigher than the mean band sharing score between mates who didnot (0.35 versus 0.25). The mean band sharing score for non-EPFdyads (0.25) was similar to the background band sharing amongnonrelatives (0.23). The mean band sharing score for mates thathad an EPF was significantly higher than that of nonrelatives(background) and was significantly lower than that of half-siblings(0.52). Our results showed a highly significant relationshipbetween genetic similarity of social mates and incidence ofEPF.