Anne E. Pusey

Inbreeding avoidance in animals

The phenomenon of inbreeding depression is well documented and behavioral adaptations for inbreeding avoidance have been described. However, there is debate over whether inbreeding depression is always an important selective force on behavior. Here, we summarize recent evidence for inbreeding depression under natural conditions, review inbreeding avoidance mechanisms, and discuss how these are influenced by social structure. We also examine the idea that animals have evolved mechanisms to avoid outbreeding.

Sex-biased dispersal and inbreeding avoidance in birds and mammals.

Sex differences in dispersal distance are widespread in birds and mammals, but the predominantly dispersing sex differs consistently between the classes. There has been persistent debate over the relative importance of two factors - intrasexual competition and inbreeding avoidance - in producing sex-biased dispersal, and over the sources of the difference in dispersal patterns between the two classes. Recent studies cast new light on these questions.

Why Lions Form Groups: Food is Not Enough

Extensive observations of foraging female lions reveal that two group sizes maximize foraging success during the season of prey scarcity: one female and five or six females. Foraging success does not vary significantly with group size when prey is abundant. Female lions live in fission-fusion social units (prides) and forage only with members of their own pride. If lion grouping patterns were primarily related to group-size-specific feeding efficiency, females in prides containing fewer than five females should forage alone when prey is scarce, whereas females in larger prides should forage alone or in groups of five or six. However, extensive data on the grouping patterns of radio-collared females show that females in small prides most commonly forage in as large a group as possible, even at the expense of foraging efficiency. Females in large prides most often forage in intermediate group sizes of four or five. However, mothers keep their cubs in a creche and form highly stable maternity groups that are effective in defending the cubs against infanticidal males. Most large prides contain a creche involving four or five mothers, and in the absence of a creche, large prides show no preference for any group size. Females also compete aggressively against neighboring prides, and larger groups successfully repel smaller ones in territorial disputes. Small prides appear to be excessively gregarious in order to compete against larger neighboring prides.

Great ape genetic diversity and population history

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

Reproductive and genetic consequences of founding isolated lion populations

Species survival is critically dependent on reproductive performance, a complex physiological process under rigorous genetic control. Classical studies of inbreeding in laboratory animals and livestock have shown that increased homozygosity can adversely affect spermatogenesis, ovulation and perinatal mortality and morbidity1–3. For wild populations, the consequences of inbreeding depression have not been examined intensively, although our recent studies of the African cheetah revealed a striking degree of genetic uniformity4,5 combined with an extremely high incidence of structurally abnormal spermatozoa (>70%) in captive6 as well as free-ranging7 males. In this study, we report definitive evidence that the reproductive function of free-ranging mammals can be impaired as a result of demographic contraction followed by inbreeding. In an examination of three distinct lion populations (two from the Serengeti ecosystem in East Africa and a third descended from lions in the Gir Forest of western India), a direct correlation was observed between genetic variability and two physiological traits, incidence of abnormal sperm and circulating testosterone, a critical hormone for spermatogenesis.

Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz

African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIVs), two of which have crossed the species barrier and generated human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2). Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts. Here we show that SIVcpz, the immediate precursor of HIV-1, is pathogenic in free-ranging chimpanzees. By following 94 members of two habituated chimpanzee communities in Gombe National Park, Tanzania, for over 9 years, we found a 10- to 16-fold higher age-corrected death hazard for SIVcpz-infected (n = 17) compared to uninfected (n = 77) chimpanzees. We also found that SIVcpz-infected females were less likely to give birth and had a higher infant mortality rate than uninfected females. Immunohistochemistry and in situ hybridization of post-mortem spleen and lymph node samples from three infected and two uninfected chimpanzees revealed significant CD4+ T-cell depletion in all infected individuals, with evidence of high viral replication and extensive follicular dendritic cell virus trapping in one of them. One female, who died within 3 years of acquiring SIVcpz, had histopathological findings consistent with end-stage AIDS. These results indicate that SIVcpz, like HIV-1, is associated with progressive CD4+ T-cell loss, lymphatic tissue destruction and premature death. These findings challenge the prevailing view that all natural SIV infections are non-pathogenic and suggest that SIVcpz has a substantial negative impact on the health, reproduction and lifespan of chimpanzees in the wild.

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.

Cooperation in male lions: kinship, reciprocity or mutualism?

Playback experiments simulating the presence of intruder male lions elicited cooperative behaviour of male coalitions resident with prides of females. Resident males approached the broadcast roars on all occasions when more than one male was present for the experiment, and only failed to approach in three of eight cases when a single male faced the roars of three intruders. Three routes to cooperation were tested: kinship, reciprocity and mutualism. These results suggest that approaching the roars of strange males is a cooperative behaviour, and that this cooperation is not conditional on either the kinship or the behaviour of a males companions. Cooperation in male lions instead appears to be based on mutualism.

Sex differences in learning in chimpanzees.

The wild chimpanzees in Gombe National Park, Tanzania, fish for termites with flexible tools that they make out of vegetation, inserting them into the termite mound and then extracting and eating the termites that cling to the tool. Tools may be used in different ways by different chimpanzee communities according to the local chimpanzee culture. Here we describe the results of a four-year longitudinal field study in which we investigated how this cultural behaviour is learned by the communitys offspring. We find that there are distinct sex-based differences, akin to those found in human children, in the way in which young chimpanzees develop their termite-fishing skills.

A comparative analysis of non-offspring nursing

Abstract Information on the incidence of non-offspring nursing in 100 mammalian species was assembled from the literature and from a questionnaire survey. A comparative analysis of these data revealed several factors that influence the occurrence of non-offspring nursing across species. The incidence of nonoffspring nursing is increased by captivity. In field studies, it is more common in species that have larger litters and there are several important differences in the context of non-offspring nursing between monotocous taxa (where females typically give birth to a single young) and polytocous taxa (where females routinely give birth to multiple young). In monotocous species, non-offspring nursing is associated with high levels of ‘milk theft’ by parasitic infants; and is more common in species where females continue nursing after they have lost their own young. In polytocous species, non-offspring nursing is not associated with ‘milk theft’ and is most common in species that live in small groups. These results are discussed in terms of the costs to females of tolerating non-offspring nursing.