Sean D. Twiss

Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies

Eight highly variable microsatellite loci were used to examine the genetic variability and differentiation of grey seals (Halichoerus grypus) at two widely spaced British breeding colonies. Samples were collected from adults and pups on the island of North Rona, off the north‐west coast of Scotland, and on the Isle of May, situated at the mouth of the Firth of Forth on the east coast Highly significant differences in allele frequencies between these two sites were found for all eight loci, indicating considerable genetic differentiation. Thus, although grey seals are known to range over very large areas outside the breeding season, site fidelity of adults and philopatry of pups for these breeding colonies must be sufficiently common to have effects, through genetic drift, at the sub‐population level. Migration rate was estimated using Wrighfs fixation index (FST), Slatkins private alleles model and the new statistic, RST, which is analogous to (FST) but which takes into account the process of microsatellite mutation. An almost 8‐fold discrepancy between the values we obtained provides cautionary evidence that microsatellite loci may contravene one or more of the assumptions on which these methods are based.

Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus)

Microsatellites were used to conduct an extensive analysis of paternity of grey seals from two Scottish breeding colonies at North Rona (n = 1189) and the Isle of May (n = 694), spanning more than a decade. A maximum of 46% of pups at North Rona and 29% of pups at the Isle of May could be allocated a father, even though the majority of candidate males for specific study sites within each colony were believed to have been sampled. Based on the paternities which could be assigned, both colonies showed evidence of reproductive skew, apparently due to the presence of approximately five males who were exceptionally successful. Some males were assigned paternities at least 10 years before, and colleagues 10 years after, being sampled, implying a reproductive lifespan of at least 10 years, and there are indications that the real maximum lies in the range 15–20 years. Male grey seals appear to have at least two breeding strategies they can adopt. On land, some males benefit from a traditionally polygynous system. However, between 50 and 70% of grey seal pups born at a particular colony are not fathered by males who are likely to be sampled by us, implying that these males seldom venture ashore here. We conclude that aquatic mating may play a much larger role in the grey seal than has previously been thought.

Male mating success and paternity in the grey seal, Halichoerus grypus: a study using DNA fingerprinting

Grey seals breed colonially on remote coastal sites. Within the colony, males compete aggressively for access to the females. We compare field observations of breeding behaviour with paternity, as determined by DNA fingerprinting, in the breeding colony on the island of North Rona. In 89% of cases where paternity was assigned, the father was observed near the mother during her perioestrous period, although in some cases this was discovered retrospectively. However, the most likely candidate male, judged on the basis of behavioural criteria, was shown not to be the father in 36% of cases. Overall, DNA typed males were more dominant, maintained positions amongst the females for longer, and accounted for disproportionately more paternities than untyped males. However, the reproductive success of the typed males is not as great as their behavioural domination of copulatory opportunities would suggest. Possible contributory factors which could explain this include: (i) imprecision in the estimates of copulatory opportunity due to mobility of males or topographical influences on individual behaviour; and (ii) opportunities for subordinate males to copulate with receptive females, either sneakily within the colony or in the water.

Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus)

Levels of parental relatedness can affect offspring survival and susceptibility to disease. We investigated parental relatedness of live and dead Halichoerus grypus pups between and within island populations and between possible causes of mortality. Nine microsatellites were used to calculate internal relatedness (IR) and standardized mean d2. We find that pups with higher than average levels of IR have significantly lower survival and that this varied between island populations and that certain loci contributed to the effect more than others. Although, there were no significant differences between causes of mortality, peritonitis, infection and stillborn had the highest levels of IR. These results provide evidence that parental relatedness is an important determinant of pre‐weaning pup survival in the grey seal and that this may vary with cause of mortality given a larger sample size.

Evidence for Mate Fidelity in the Gray Seal

Colonially breeding gray seals are polygynous. Males are larger than females, compete with each other for position among aggregated females, and contribute no parental care. Genetic analysis of pups born on the island of North Rona, Scotland, reveals large numbers of full siblings, although dominant males father disproportionately few of these. This result cannot be explained by mating patterns based solely on male dominance and the spatio-temporal organization of the breeding colony. Instead, many full siblings must result from choices favoring previous parental combinations. Thus, polygyny and partner fidelity appear to operate simultaneously in this breeding colony.

The impact of climatic variation on the opportunity for sexual selection.

Many studies have demonstrated influences of climatic variation on a variety of ecological processes, however, its impact on the potent evolutionary force of sexual selection has largely been ignored. The intensity of sexual selection is a fundamental parameter in animal populations, which depends upon the degree of polygamy and will probably be influenced by the impact of local climatic variation upon ‘environmental potential for polygamy’. Here, we provide evidence of a direct effect of local climatic variation on the intensity of sexual selection, by showing a clear correlation between local weather conditions and inter-annual changes in the degree of polygamy in a long-term study of colonially breeding grey seals (Halichoerus grypus). Our results show that changes in local weather conditions alter the annual proportion of males contributing to the effective population size (Ne) by up to 61%. Consequently, over the ‘lifetime’ of a cohort, a broader range of individuals will contribute genetically to the next generation if local weather conditions are variable. In the context of predicted future changes in climatic variation, these findings have broad implications for population genetics of socially structured animal systems through the major influence that the degree of polygamy has upon Ne.

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.

Finding fathers: spatio‐temporal analysis of paternity assignment in grey seals (Halichoerus grypus)

Molecular studies of pinniped breeding systems exhibit a broad range of agreement and disagreement with observational indices of male breeding success. Grey seal studies have reported considerable discrepancies between genetic and behavioural paternity measures that have been interpreted as evidence of previously unidentified male strategies and/or tactics. Therefore, these studies have the power to fundamentally alter our perceptions of mating systems. However, other pinniped studies exhibit no such disagreements, and one possible explanation for disparities may be sampling biases in space and time. Therefore, it is essential that potential sampling biases are examined to evaluate the likelihood of previously unidentified male strategies. We examined paternities assigned at the North Rona grey seal colony between 1999 and 2002 in relation to concurrent detailed behavioural and locational data for males and females. We found that (i) for females observed in sexual interaction(s) during their oestrus period, it was highly probable that one of the interacting males fathered their next pup; (ii) over 80% of assigned paternities agreed with observations of the in‐colony behaviour and spatio‐temporal proximity of the males and females involved; and (iii) a minority of females exhibit mate choice and seek sires outside their local males home range, although evidence suggests that these females mate on the colony rather than at sea. In conclusion, nearly all paternities assigned agreed with expectation based upon detailed knowledge of the spatio‐temporal patterns of individuals during the breeding season. We found little evidence of unidentified male strategies at North Rona, Scotland, whereas further examination of mechanisms of female choice may be productive.

Finescale topographical correlates of behavioural investment in offspring by female grey seals, Halichoerus grypus.

Grey seals breed colonially on substrates ranging from ice to rocky or sandy beaches. Clear differences in seal behaviour patterns exist among such broad classes of breeding habitat. However, finer scale topographical variation is likely to influence individual behaviour with consequences for pupping success. We examined topographical influences on the behaviour of breeding female grey seals by quantifying topography at a subseal size resolution. Using submetre resolution digital terrain models of two sites within a rocky breeding colony, we compared site topography in relation to observed differences in female behaviour at these sites. Females at both sites preferred breeding close to water (standing pools or sea) and frequently commuted between their pups and water. Topographical models indicated that one site was more costly for seals in terms of their locations and movements within the site. This was due to a lack of low-elevation land adjacent to the main access points from the sea and the reduced availability of pools. Females at this site showed reduced pup attendance and an increase in energetically costly behaviours, whilst females at the lower-cost site spent more time interacting with their pups and resting. These topographically induced behavioural differences are likely to affect the quantity and quality of pup provisioning by mothers and influence individual pupping site selection. Less costly sites are likely to be colonized preferentially and by larger, older and more dominant females, potentially generating finescale spatial heterogeneity in female quality within the breeding colony. Copyright 2000 The Association for the Study of Animal Behaviour.

Reproductive performance links to fine-scale spatial patterns of female grey seal relatedness

Fine–scale spatial patterns of female relatedness throughout the established grey seal breeding colony of North Rona, Scotland, were investigated by accurate mapping and spatially explicit analyses of a large sample (n=262) of mothers using variation at nine microsatellite DNA loci. Local spatial autocorrelation analyses identified locations where seals were more highly related to the colony than average. These locations were also areas where the more successful females bred, were occupied first during each breeding season, were centrally placed locations of preferred habitat types and were likely to be the locations which were the first to be colonized historically. Mothers occupying such sites achieved higher than average pup growth rates, suggesting a founder fitness benefit.