Mating system and reproductive success in eastern Pacific harbour seals

Harbour seals sometimes breed along inland travel corridors where females become clustered in space and time and males establish underwater acoustic display territories similar to terrestrial arenas known as resource-based leks. Under these conditions, we predicted that higher levels of polygyny would be observed than has been previously reported for this species mating in open coast environments without travel corridors. Reproductive success (RS) of 70 males was measured using 20 microsatellite DNA loci and likelihood-based paternity analysis of 136 offspring collected over 3 years. Most males were assigned either zero or one paternity with 80% confidence. The greatest number of pups assigned to one male in a season was two. Variance in RS was higher for males than females (which are biologically limited to one offspring per year) indicating low to mild polygyny. In addition, distributions of relatedness values among pups within year classes did not differ significantly from a simulated distribution with R = 0, indicating that half-siblings were uncommon. Overall, polygyny levels were low relative to terrestrial pinniped mating systems and similar to observations from a harbour seal population along an open coast. Due to large confidence intervals associated with our results, we cannot rule out the hypothesis that a travel corridor might increase the degree of polygyny skew relative to that observed in open coast environments. Habitat appeared to influence male strategies as the most successful males in open coast environments patrolled offshore, while the most successful male in this study defended a territory along the travel corridor.     

Weak polygyny in California sea lions and the potential for alternative mating tactics

Female aggregation and male territoriality are considered to be hallmarks of polygynous mating systems. The development of genetic parentage assignment has called into question the accuracy of behavioral traits in predicting true mating systems. In this study we use 14 microsatellite markers to explore the mating system of one of the most behaviorally polygynous species, the California sea lion (Zalophus californianus). We sampled a total of 158 female-pup pairs and 99 territorial males across two breeding rookeries (San Jorge and Los Islotes) in the Gulf of California, Mexico. Fathers could be identified for 30% of pups sampled at San Jorge across three breeding seasons and 15% of sampled pups at Los Islotes across two breeding seasons. Analysis of paternal relatedness between the pups for which no fathers were identified (sampled over four breeding seasons at San Jorge and two at Los Islotes) revealed that few pups were likely to share a father. Thirty-one percent of the sampled males on San Jorge and 15% of the sampled males on Los Islotes were assigned at least one paternity. With one exception, no male was identified as the father of more than two pups. Furthermore, at Los Islotes rookery there were significantly fewer pups assigned paternity than expected given the pool of sampled males (p<0.0001). Overall, we found considerably lower variation in male reproductive success than expected in a species that exhibits behavior associated with strongly polygynous mating. Low variation in male reproductive success may result from heightened mobility among receptive females in the Gulf of California, which reduces the ability of males to monopolize groups of females. Our results raise important questions regarding the adaptive role of territoriality and the potential for alternative mating tactics in this species.     

Low reproductive success in territorial male Antarctic fur seals (Arctocephalus gazella) suggests the existence of alternative mating strategies

Microsatellites were used to conduct an analysis of paternity of Antarctic fur seals (Arctocephalus gazella) from Bird Island, South Georgia. At most, only 28% of pups at our study site could be assigned a father, even though the majority (approximately 90%) of candidate males within this colony were sampled. The behavioural and genetic evidence from this study suggests that a number of alternative mating strategies may exist within this fur seal population. Holding a land-based territory conferred an advantage to male reproductive success. However, this advantage was much smaller than expected from behavioural observations. At least 70% of fur seal pups born at our study site in a given year are not fathered by males who held a territory or were observed copulating with females in the previous year, implying that there exists a pool of males that seldom venture ashore at this site. To explain this discrepancy we suggest that female choice is an integral component of the Antarctic fur seal mating system and that aquatic mating may play a much larger role in the Antarctic fur seal than previously thought.     

The rate of fertilization in male mating tactics of the polygynous grey seal

Studies using molecular markers have shown that some grey seal males may be gaining success through exhibiting alternative mating tactics. We estimated the probability of fertilization success of grey seal males exhibiting the primary tactic of female defence and one alternative tactic of mating with departing females on Sable Island, Nova Scotia, Canada, during the breeding seasons of 1997-2002. Although the fertilization rate of the primary tactic (27-43%) was greater than that of the alternative tactic (10-12%), these low rates indicate the potential fitness value of alternative mating tactics in this size-dimorphic pinniped species.     

Genetic analysis of the mating system of the common brushtail possum (Trichosurus vulpecula) in New Zealand farmland

We examined male reproductive success in a common brushtail possum population in New Zealand farmland. Paternity was assigned to 66 of 91 pouch young (maternity known), using a likelihood approach applied to genotypes at six microsatellite loci having an overall average exclusion probability of around 99%. The distribution of number of offspring per male was L-shaped with a standardized variance of 1.52. At least 46% of the 76 sampled reproductively mature males, bred, siring between one and four offspring each. Although breeding males were on average older and larger than nonbreeding males, the small differences did not result in a significant overall difference between the two groups in a multivariate permutation test analagous to a t-test. Paternity analysis of 22 sibling pairs (resulting from experimental removal of pouch young early in the breeding season, inducing a second oestrous) suggested that sequential mating of females with the same male was uncommon ( approximately 16-27%). Whilst there was a tendency for female possums to mate with nearby males, consistent with previous observations of territorial mating behaviour in Australian populations, some interhabitat matings were also inferred. The study population displayed only a low degree of polygyny, which may in part reflect population and habitat characteristics of the study site. A comprehensive understanding of the mating system of Trichosurus vulpecula awaits genetic paternity analysis in additional populations from both Australia and New Zealand, using quantitative approaches undertaken in this study.     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

Factors influencing and consequences of breeding dispersal and habitat choice in female grey seals (<Emphasis Type="Italic">Halichoerus grypus</Emphasis>) on Sable Island,Nova Scotia

Selection of breeding location can influence reproductive success and fitness. Breeding dispersal links habitat use and reproduction. This study investigated factors affecting breeding dispersal and its reproductive consequences in grey seals (Halichoerus grypus) on Sable Island, Nova Scotia. Breeding dispersal distance was determined in 692 individually marked, known-age female grey seals observed from 2004 to 2014. We used generalized linear mixed-effects models to test hypotheses concerning environmental and demographic factors influencing breeding dispersal distance and the consequences of dispersal distance on offspring weaning mass. Grey seal females rarely exhibited fidelity to previous breeding sites. Median dispersal distance between years was 5.1 km. Only 2.9% of females returned to a previous breeding site. Breeding dispersal distance was affected by parity and density, but effects were small and are presumably of no biological significance. Variation in dispersal distance among adult females was large. Dispersal distance had no significant influence on offspring weaning mass; however, as previously found, pup sex and maternal age did. Although breeding location was not important, heavier pups were born in habitats with no tidal or storm-surge influence indicating that breeding habitat type did influence offspring size at weaning. The lack of site fidelity in grey seals on Sable Island is associated with an unpredictable and changing landscape (sand dunes) that could make it difficult for females to locate previous breeding locations. Although breeding location within habitat type had small consequences on offspring weaning mass, we detected no evidence that breeding site selection within the habitat had consequences to females.     

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.     

Female distribution, genetic relatedness, and fostering behaviour in harbour seals, Phoca vitulina

Although harbour seals may not recognize their relatives, relatives could be chosen preferentially for fostering (i.e. kin selection) if harbour seals display natal philopatry coupled with breeding site fidelity, and thus kin are clustered within the colony. We used behavioural and genetic data to investigate population structure within the Sable Island breeding colony and to test whether harbour seals tend to foster related pups. Adult females on Sable Island showed a high level of breeding-colony site fidelity but low levels of within-colony site fidelity both within and between years. Similarly, although lactating females showed a clumped distribution, group composition was highly variable, suggesting that this study colony was not composed of groups of related animals. DNA fingerprint data supported the hypothesis that female distribution within the colony was not correlated with genetic relatedness. Furthermore, the mean DNA band sharing among foster dyads did not differ significantly from that for unrelated animals. These results indicate that among harbour seals, related pups are not usually chosen preferentially for fostering and hence, kin selection is not likely to be influencing the occurrence of this behaviour. Copyright 1999 The Association for the Study of Animal Behaviour.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

The association between rank,mating effort,and reproductive success in male Barbary macaques (Macaca sylvanus)

The association between social rank, mating effort, and reproductive success of male Barbary macaques (Macaca sylvanus) has been evaluated by longterm behavioral observations and subsequent paternity determination via oligonucleotide DNA fingerprinting in a large semifreeranging group. All offspring born between 1985 and 1988 that survived to at least 1 year of age (n=75) were available for paternity testing. The exclusion of all but one of the potential fathers from paternity was possible in 70 cases (93%). Mating activities were recorded using ad lib. and focal female sampling techniques. The analysis of male mating effort was restricted to the most likely days of conception. Male rank correlated significantly with male mating success in all four breeding seasons and with male reproductive success in three of the four seasons. Mating success and reproductive success also showed a significant correlation, with the exception of one breeding season, in which the proportion of males per fertilizable female was especially high. Poor mating success was almost always associated with poor reproductive success, while good mating success was less predictive for a male's actual reproductive success. This was apparently a consequence of sperm competition, resulting from the promiscuous mating system. Male mating success is not necessarily an unreliable indicator for reproductive success, provided that sufficient sample sizes are available and that conception periods can be determined. Sperm competition and other factors may weaken the association, however.     

Early male reproductive advantage,multiple paternity and sperm storage in an amphibian aggregate breeder

We tested whether the order in which males encounter females affects reproductive fitness in spotted salamanders (Ambystoma maculatum). Using mating chambers in the field, we allowed one male access to a female before a second male. We then used four microsatellite markers in paternity analyses of the resulting larvae. First males sired a significantly larger number of offspring than second males, suggesting that male reproductive success is greatly enhanced by early arrival at breeding ponds. Multiple paternity was common among clutches, and frequently larvae were assigned to unidentified males that had not been in the chambers. Sperm from these males had either been stored by females for a year or obtained more recently at other breeding sites.     

Molecular determination of paternity in a natural population of the multiply mating polygynous lizard Eulamprus heatwolei

We studied the mating system of the southern water skink, Eulamprus heatwolei, during spring and summer (encompassing the breeding season) in a population in southeastern Australia. We examined potential attributes that might influence the mating system and male reproductive success including home range size, physical proximity of adults and body size, and then genotyped all mothers, offspring and potential sires. Home range overlap of both sexes was extensive, with adult females sharing the greatest amount of space with each other and adult males the least amount of space with each other. However, not all adults hold home ranges. We classified approximately one quarter of adult males as home range holders and the rest as 'floaters'. Adult females occupy home ranges more than males, with approximately three-quarters classified as home range holders. Home range ownership is not correlated with body size for either sex, however, male body size is positively correlated with the number of adult female home ranges that his home range overlaps and adult male home ranges are larger than those of females. We used microsatellite genotyping to assign paternities to 55 offspring from 17 litters and then compared this data with our home range and behavioural observations. This species displays extreme levels of multiple paternity given the small mean clutch size of three. Multiple paternity was confirmed in 11 (64.7%) of 17 clutches but three other clutches (for a total of 82.4%) also may display multiple paternity. A total of 30 offspring from 12 litters were assigned to 10 of the 32 genotyped adult males from our study site. Of these 10 adult males, half were home range holders. Five complete clutches and a total of 25 out of the 55 offspring could not be positively assigned to any male surveyed as part of the study and were attributed to floater males or resident males adjacent to our study site that had not been genotyped. While sample sizes are small, neither male home range ownership nor body size is significantly correlated with the number of paternities a male obtained. Our study suggests a polygynous mating system for this species.     

Changes in body mass and feeding behaviour in male harbour seals, Phoca vitulina, in relation to female reproductive status

Loss of body mass has been used as an index of the cost of reproductive effort in mammals. We studied changes in body mass of male harbour seals, Phoca vitulina , during the breeding season on Sable Island, Nova Scotia, Canada. Individually marked subadult ( n = 21) and adult ( n = 22) males were captured at approximately six-day intervals throughout the breeding season. Adult males weighed an average of 108 kg ± 5·6 (S.E.) at initial capture, whereas subadults weighed an average of 76 ± 6·6 kg. The rate of mass loss by adult males did not differ from zero during the pre-mating period (i.e. the period without receptive females), but differed significantly from zero (-0·91 ± 0·007 kg/day) during the mating period (i.e. the period with receptive females). By contrast, the rate of mass change of subadults did not differ from zero in either period, indicating that food availability was unlikely to be responsible for the observed changes in adults. Adult males lost up to 24% of body mass during the breeding season. Examination of sera for the presence of chylomicrons (i.e. evidence of recent feeding) also suggested that adults stopped feeding during the mating period, while subadults did not. These results suggest that reproduction represents a significant energetic cost to adult male harbour seals.     

Multiple mating strategies explain unexpected genetic mixing of New Zealand fur seals with two congenerics in a recently recolonized population

Human impacts on natural systems can cause local population extinctions, which may promote redistribution of taxa and secondary contact between divergent lineages. In mammalian populations that have mating systems shaped by polygyny and sexual selection, the potential for hybridization to ensue and persist depends on individual and demographic factors. At Macquarie Island, a recently formed fur seal population is comprised of both sexes of breeding Antarctic (Arctocephalus gazella) and subantarctic (A. tropicalis) fur seals, and an itinerant collection of male New Zealand fur seals (A. forsteri), presumed to be non-breeders due to their absence from principle breeding areas. The mating system of the three species is described as resource-defence polygyny: males defend beach territories containing breeding females for exclusive mating rights. A recent genetic study identified a high level of hybridization in the population (17-30%), unexpectedly involving all three species. This study examined the source of involvement in breeding by A. forsteri with respect to mating strategies operating in the population. Ninety-five (10%) pups born from 1992 to 2003 were genetically identified as New Zealand hybrids. Most resulted from reproduction within territories by New Zealand hybrids of both sexes, although some were conceived extra-territorially, indicating that males successfully utilize strategies other than territory holding to achieve paternities. Female reproductive status influenced mating partner and mating location, and females without pups were more likely to conceive extra-territorially and with A. forsteri males. This study illustrates an important consequence of low heterospecific discrimination in a sympatric population of long-lived mammals.     

Noninvasive paternity assignment in Gombe chimpanzees

The relative success of chimpanzee male mating strategies, the role of male dominance rank and the success of inbreeding avoidance behaviour can only be assessed when paternities are known. We report the probable paternities of 14 chimpanzees included in a long‐term behavioural study of chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. DNA samples were collected noninvasively from shed hair and faeces and genotyped using 13–16 microsatellite loci characterized in humans. All 14 offspring could be assigned to fathers within the community. While there is a positive relationship between male rank and reproductive success, we demonstrate that a range of male mating strategies (possessiveness, opportunistic mating and consortships) can lead to paternity across all male ranks. Several adult females were at risk of breeding with close male relatives. Most successfully avoided close inbreeding but in one case a high‐ranking male in the community mated with his mother and produced an offspring. In contrast to recent data on chimpanzees (P. t. verus) from the Taï forest, Côte d’Ivoire, no evidence of extra‐group paternity was observed in our study. Reanalysis of Taï data using a likelihood approach casts doubt on the occurrence of extra‐group paternity in that community as well.     

A multivariate analysis of phenotype and paternity in male harbor seals, Phoca vitulina, at Sable Island, Nova Scotia

Understanding the links between phenotype and reproductive successis critical to the study of the evolution of mating systemsand life-history patterns. We examined the relationship betweenphenotype and mating success of male harbor seals (Phoca vitulinaconcolour) at Sable Island, Canada. Cluster analyses of eighttraits including mating success determined by genetic paternityanalysis, haul-out behavior, body mass, and mass change identifiedfour groups of males with distinct characteristics. The most successfulmales were of moderate body size, were rarely sighted alone,were associated with many different groups on shore, and weresighted on the haul-out relatively infrequently. Large malesthat hauled out frequently alone, previously thought to be sociallydominant, were less likely to be successful. Also less successfulwere smaller, younger males. Contrary to our hypotheses, andunlike most terrestrially breeding pinnipeds, body size and reproductiveeffort were not positively associated with mating success, and somesuccessful males appeared to spend considerable time foragingin deep water.     

The implications of stress on male mating behavior and success in a sexually dimorphic polygynous mammal, the grey seal

Studies on primates and other taxa have shown that the physiological response of an individual to stress reflects their social status. We combined behavioral observations with measures of stress to test the hypothesis that stress is an important physiological determinant of mating behavior and success in the male grey seal. Known-age males (N=19) were studied during the breeding seasons of 2004 and 2005 at Sable Island, Canada. The stressor was a capture and restraint period of 35 min and serial samples of cortisol and testosterone were taken as measures of stress. The mean baseline concentrations of cortisol and testosterone were 9.7+/-0.5 ug/dl and 6.2+/-0.6 ng/mL, respectively. The baseline cortisol concentration was negatively correlated with the duration of time a male spent at a site (r=-0.507, P=0.027), which was a strong correlate of mating success (r=0.659, P=0.002). All males experienced an increase in the concentration of cortisol during the restraint period (79.1+/-8.4%; CV=46.1%). The percentage rise in cortisol during restraint was correlated with the mean duration of time spent at a site (r=0.544, P=0.016) and thus success. The concentration of testosterone also increased during the restraint period (32.8+/-9.7%). This might be an adaptive response to maintaining the ability to reproduce while under stress. Our study indicates that stress is an important determinant of success in male grey seals. More successful males might exhibit an adaptive response to stress by maintaining low concentrations of cortisol during breeding.     

Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction

Human-induced changes to natural systems can cause major disturbances to fundamental ecological and population processes and result in local extinctions and secondary contacts between formerly isolated species. Extensive fur seal harvesting during the nineteenth century on Macquarie Island (subantarctic) resulted in extinction of the original population. Recolonization by three species has been slow and complex, characterized by the establishment of breeding groups of Antarctic and subantarctic fur seals (Arctocephalus gazella and Arctocephalus tropicalis) and presumed nonbreeding (itinerant) male New Zealand fur seals (Arctocephalus forsteri). One thousand and seven pups from eight annual cohorts (1992-2003) were analysed using mitochondrial control region data (RFLP) and 10 microsatellite loci to estimate species composition and hybridization. Antarctic fur seals predominated, but hybridization occurred between all three species (17-30% of all pups). Involvement of New Zealand fur seals was unexpected as females are absent and males are not observed to hold territories during the breeding season. The proportion of hybrids in the population has fallen over time, apparently owing to substantial influxes of pure Antarctic and subantarctic individuals and non-random mating. Over 50% of New Zealand hybrids and 43% of Antarctic-subantarctic hybrids were not F(1), which indicates some degree of hybrid reproductive success, and this may be underestimated: simulations showed that hybrids become virtually undetectable by the third generation of backcrossing. While human impacts seem to have driven novel hybridization in this population, the present 'time slices' analysis suggests some biological resistance to complete homogenization.     

Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara)

Captive breeding is an integral part of many species recovery plans. Knowledge of the genetic mating system is essential for effective management of captive stocks and release groups, and can help to predict patterns of genetic diversity in reintroduced populations. Here we investigate the poorly understood mating system of a threatened, ancient reptile (tuatara) on Little Barrier Island, New Zealand and discuss its impact on the genetic diversity. This biologically significant population was thought to be extinct, due to introduced predators, until 8 adults (4 males, 4 females) were rediscovered in 1991/92. We genotyped these adults and their 121 captively-bred offspring, hatched between 1994 to 2005, at five microsatellite loci. Multiple paternity was found in 18.8% of clutches. Male variance in reproductive success was high with one male dominating mating (77.5% of offspring sired) and one male completely restricted from mating. Little Barrier Island tuatara, although clearly having undergone a demographic bottleneck, are retaining relatively high levels of remnant genetic diversity which may be complemented by the presence of multiple paternity. High variance in reproductive success has decreased the effective size of this population to approximately 4 individuals. Manipulation to equalize founder representation was not successful, and the mating system has thus had a large impact on the genetic diversity of this recovering population. Although population growth has been successful, in the absence of migrants this population is likely at risk of future inbreeding and genetic bottleneck.