Russell C. Van Horn

Can't get there from here: inferring kinship from pairwise genetic relatedness

*Department of Biology, Duke UniversityyDepartment of Ecology and Evolutionary Biology, Princeton UniversityzInstitute of Primate Research, National Museums of Kenya(Received 17 May 2007; initial acceptance 7 June 2007;final acceptance 26 August 2007; published online 28 January 2008; MS. number: AS-1316R)

Behavioural structuring of relatedness in the spotted hyena ( Crocuta crocuta ) suggests direct fitness benefits of clan-level cooperation

Spotted hyenas (Crocuta crocuta) are gregarious carnivores that live in multigenerational social groups, called clans, containing one to several matrilines. Members of multiple matrilines within a clan cooperate during dangerous interactions with inter‐ and intraspecific competitors. The evolution of cooperation may be influenced by relatedness between individuals, which in turn is influenced by reproductive skew and mate choice, dispersal and territorial behaviours. Behavioural data exist for spotted hyenas, but corresponding data on patterns of relatedness are unavailable; this lack of data makes it difficult to assess the relative importance of selection pressures favouring cooperative behaviour within and among groups. Therefore we conducted a longitudinal analysis of relatedness within a single large clan of spotted hyenas, as well as a cross‐sectional analysis of relatedness among hyenas from multiple clans. Within a clan, patterns of relatedness reflected known pedigree relationships, and relatedness was higher within than among matrilines, even across generations. Although mean within‐matriline relatedness varied among matrilines, it did not decline with matriline rank. On average, clan members were not related closely, due to high levels of male‐mediated gene flow among clans, and relatedness declined very slightly across clan borders. Low mean relatedness within clans suggests that spotted hyenas cooperate with unrelated clan‐mates against close paternal kin in other clans. Our data also suggest that spotted hyenas must derive large net direct fitness benefits from group living and cooperation.

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called ‘clans’, resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group‐mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group‐mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon‐like sociality among top‐level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio‐ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species’ range, and describe the long‐term fitness consequences of rank‐related variation in resource access among clan‐mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non‐kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year‐round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.

Association patterns among male and female spotted hyenas (Crocuta crocuta) reflect male mate choice

Abstract. Although female animals tend to be choosier than males in selecting mates, sexual selection theory predicts that males should also be choosy when female fecundity varies. Reproductive success among female spotted hyenas varies greatly with social rank. Our goals were therefore to determine whether male hyenas preferentially associate with high-ranking females, and whether male preferences are affected by female reproductive state. Interactions between adult males and females were observed intensively, and association indices calculated for all male-female pairs, over a 7-year period in one population of free-living hyenas. Males initiated most affiliative interactions with females, and males associated most closely with females that were likeliest to be fertile. High- and middle-ranking males associated most closely with high-ranking females, but low-ranking males associated equally closely with females in all rank categories. We used molecular markers to determine the paternity of cubs born during the study period, and found that sires associated more closely with the mothers of those cubs than did non-sires, particularly during the last months before conception. These association data indicate that male spotted hyenas do indeed exhibit selective mate choice, and that they prefer females likeliest to maximize male reproductive success.

Kin discrimination in the spotted hyena (Crocuta crocuta): Nepotism among siblings

We examined patterns of affiliation, association, and aggression to inquire whether spotted hyenas (Crocuta crocuta) can distinguish among various groups of maternal and paternal siblings. If so, and if these animals conform to predictions of kin selection theory, then behavioral interactions among hyenas should vary with relatedness. We also considered familiarity-based recognition and phenotype matching as mechanisms hyenas might use to recognize kin. Patterns of affiliative behavior indicated that hyenas favored full-sibling littermates over half-sibling littermates or any other group of half-siblings. Rates of dyadic aggression generally did not vary with kinship. Hyenas associated more closely with half-sibling littermates than with non-littermate half-siblings, and hyenas affiliated more with maternal half-siblings than with paternal half-siblings, suggesting that familiarity-based cues might mediate discrimination among these sibling classes. In addition, operation of a phenotype-matching mechanism was suggested by the preference hyenas demonstrated during affiliative interactions for full- over half-sibling littermates, and by their lack of preference in these interactions for half-sibling littermates over non-littermate half-siblings. Phenotype matching was also suggested by our observation that paternal half-siblings cooperated more, and fought less, than did non-kin. Our data indicate that hyenas can discriminate among various types of siblings, that their social behavior conforms to predictions of kin selection theory, and that they recognize kin using mechanisms of both familiarity and phenotype matching.

Friendships between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus).

Close associations between adult males and lactating females and their dependent infants are not commonly described in non-monogamous mammals. However, such associations [sometimes called “friendships” (Smuts 1985)] are regularly observed in several primate species in which females mate with multiple males during the fertile period. The absence of mating exclusivity among “friends” suggests that males should invest little in infant care, raising questions about the adaptive significance of friendship bonds. Using data from genetic paternity analyses, patterns of behavior, and long-term demographic and reproductive records, we evaluated the extent to which friendships in four multi-male, multi-female yellow baboon (Papio cynocephalus) groups in Amboseli, Kenya represent joint parental care of offspring or male mating effort. We found evidence that mothers and infants benefited directly from friendships; friendships provided mother–infant dyads protection from harassment from other adult and immature females. In addition, nearly half of all male friends were the genetic fathers of offspring and had been observed mating with mothers during the days of most likely conception for those offspring. In contrast, nearly all friends who were not fathers were also not observed to consort with the mother during the days of most likely conception, suggesting that friendships between mothers and non-fathers did not result from paternity confusion. Finally, we found no evidence that prior friendship increased a male’s chances of mating with a female in future reproductive cycles. Our results suggest that, for many male–female pairs at Amboseli, friendships represented a form of biparental care of offspring. Males in the remaining friendship dyads may be trading protection of infants in exchange for some resources or services not yet identified. Our study is the first to find evidence that female primates gain social benefits from their early associations with adult males.

AGE ESTIMATION AND DISPERSAL IN THE SPOTTED HYENA (CROCUTA CROCUTA)

Abstract We used observations of known-age, free-ranging spotted hyenas (Crocuta crocuta) from a large social group to develop age-estimation models. A model based on tooth-eruption data estimates the ages of animals 10.0–15.5 (±1.1 SD) months old. We used tooth-wear data to estimate the ages of adult males ±4.9 months and ages of females ±22.6 months. Analysis of known and estimated ages shows that males usually disperse from their natal group when 24–60 months of age. Eight of 20 males whose fates were known lived in 3 groups over time, and at least 7 of 41 resident immigrant males appeared to arrive in the study group years after leaving their birthplaces. Thus, males of this species often engage in multiple dispersal events.

Divided destinies: group choice by female savannah baboons during social group fission

Group living provides benefits to individuals while imposing costs on them. In species that live in permanent social groups, group division provides the only opportunity for nondispersing individuals to change their group membership and improve their benefit to cost ratio. We examined group choice by 81 adult female savannah baboons (Papio cynocephalus) during four fission events. We measured how each female’s group choice was affected by several factors: the presence of her maternal kin, paternal kin, age peers, and close social partners, her average kinship to groupmates, and her potential for improved dominance rank. Maternal kin, paternal kin, and close social partners influenced group choice by some females, but the relative importance of these factors varied across fissions. Age peers other than paternal kin had no effect on group choice, and average kinship to all groupmates had the same effect on group choice as did maternal kin alone. Most females were subordinate to fewer females after fissions than before, but status improvement did not drive female group choice; females often preferred to remain with social superiors who were their close maternal kin, rather than improving their own social ranks. We suggest that during permanent group fissions, female baboons prefer to remain with close maternal kin if those are abundant enough to influence their fitness; if they have too few close maternal kin then females prefer to remain with close paternal kin, and social bonds with nonkin might also become influential.

Antibodies to canine and feline viruses in spotted hyenas (Crocuta crocuta in the masai mara national reserve

Spotted hyenas (Crocuta crocuta) are abundant predators in the Serengeti ecosystem and interact with other species of wild carnivores and domestic animals in ways that could encourage disease transmission. Hyenas also have a unique hierarchical social system that might affect the flow of pathogens. Antibodies to canine distemper virus (CDV), feline immunodeficiency virus (FIV), feline panleukopenia virus/canine parvovirus (FPLV/CPV), feline coronavirus/feline infectious peritonitis virus (FECV/FIPV), feline calicivirus (FCV), and feline herpesvirus 1 (FHV1) have been detected in other Serengeti predators, indicating that these viruses are present in the ecosystem. The purpose of this study was to determine whether spotted hyenas also had been infected with these viruses and to assess risk factors for infection. Serum samples were collected between 1993 and 2001 from 119 animals in a single clan for which behavioral data on social structure were available and from 121 hyenas in several other clans. All animals resided in the Masai Mara National Reserve. Antibodies to CDV, FIV, FPLV/CPV, FECV/FIPV, FCV, and FHV1 were present in 47%, 35%, 81%, 36%, 72%, and 0.5% of study hyenas, respectively. Antibody prevalence was greater in adults for FIV and FECV/FIPV, and being a female of high social rank was a risk factor for FIV. Hyenas near human habitation appeared to be at lower risk to have CDV, FIV, and FECV/FIPV antibodies, whereas being near human habitation increased the risk for FPLV/CPV antibodies. Canine distemper virus and FECV/FIPV antibody prevalence varied considerably over time, whereas FIV, FPLV/CPV, and FCV had a stable, apparently endemic temporal pattern. These results indicate that hyenas might play a role in the ecology of these viruses in the Serengeti ecosystem. The effect of these viruses on hyena health should be further investigated. The lower prevalence of CDV antibody–positive hyenas near human habitation suggests that reservoirs for CDV other than domestic dogs are present in the Serengeti ecosystem.

Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta)

Observational and telemetry data were used in a geographic information system database to document the ontogenetic development of sexually dimorphic patterns of space use among free-living spotted hyenas Crocuta crocuta in Kenya. No measures of space use were sexually dimorphic among den-dwelling cubs, nor were sex differences apparent among hyenas that had ceased using dens for shelter until these animals were c. 30 months of age. Significant sex differences emerged late in the third year of life, and persisted throughout the remainder of the life span; males were found farther from the geographic centre of the natal territory than were females, and the mean size of individual 95 % utility distributions was larger for males than females. Most dispersal events by radio-collared males were preceded by a series of exploratory excursions outside the natal territory. All collared males dispersed, but no collared females did so. Most dispersing males moved only one or two home ranges away at dispersal, roughly 8–10 km distant from the natal territory, before settling in a new social group.