Integrating molecular techniques with field methods in studies of social behavior: a revolution results

Ecology, March, 1998 by Colin Hughes

Dominance hierarchies are conspicuous features of many animal social groups. Individuals are presumed to contend for high dominance rank because it confers access to mates or breeding status. Parentage assignment using molecular markers has confirmed this presumption in some species, but in other species there is no clear relationship. Dominance status and male access to females inferred from behavioral observations of savannah baboons, Papio cyanocephalus, accurately predicted genetic relationships identified through DNA fingerprinting (Altmann et al. 1996). Behavioral observation overestimated reproductive success of dominant grey seals, Halichoerus gryphus, consistent with furtive behavior of subordinates (Amos et al. 1993b). Alpha male rhesus macaques, M. mulatta, were able to monopolize reproduction, too, at least in small groups (Melnick et al. 1984, Melnick 1987), but three other studies suggest caution in assuming that high dominance rank automatically confers high reproductive success. Under controlled conditions, alpha-male poeciliids, Limia perugiae, dominated reproduction in small groups but failed to reproduce in large groups (Schartl et al. 1993). In a study of three social groups of Pukekos, Porphyrio porphyrio melanotus, no relationship was found between dominance status and reproduction. Indeed, in one group, the alpha male fathered none of the 14 chicks hatched over three seasons (Lambert et al. 1994). In Barbary macaques, Macaca sylvanus, there was little reproductive dominance by the "alpha" male, and most males in a group sired offspring (von Segesser et al. 1995). The caution sounded by Millar et al. (1994) and Altmann et al. (1996) about interpretation of studies based on a limited part of the reproductive lifetime are particularly pertinent here; more work is required before abandoning the theory that animals fight for high dominance rank because it confers higher fitness. The data indicate that the size of the group in which an individual lives may be especially important in the dynamic relationship between its dominance status and its reproductive success.

Identification of group structure

In other social animals, individual identification and close behavioral observation are so difficult that molecular methods represent the only feasible approach to understanding their behavior. One of the first such studies was the investigation of the huge nursery colonies of Mexican free-tailed bats, Tadarida brasiliensis (McCracken 1984). McCracken used allozymes to show that females find and nurse their own pups most of the time, contrary to previous statements about indiscriminate nursing. This has been confirmed in other species of bats using DNA fingerprinting (Bishop et al. 1992, Watt and Fenton 1995). In lions, Panthera leo, long lifespan and low population density make it difficult to study a large sample of individuals over their lifetimes, let alone a sample of prides over the lives of all lions in those groups. DNA fingerprinting readily confirmed kinship among females within prides and revealed details of relatedness among males that form coalitions. Large coalitions of males are much more likely to consist of relatives than small coalitions (Packer et al. 1991). Though larger coalitions are more successful in taking over prides, it becomes increasingly unlikely, as size of coalition increases, that each individual male will mate following a takeover. Related males in larger coalitions will still benefit indirectly through reproduction of their male relatives. Naked mole-rats, Heterocephalus glaber, are African rodents that attract attention by being the only eusocial mammals, but defy study by their entirely fossorial life style (Jarvis et al 1994). DNA fingerprinting of individuals caught from wild colonies revealed intense inbreeding within colonies and high genetic similarity among colonies. These results are consistent with near-zero dispersal and colony formation by fission (Reeve et al. 1990). Whales are, perhaps, the epitome of difficult study subjects; Amos and colleagues have taken advantage of the opportunity presented by Faroese whale hunts where whole pods of long-finned pilot whales, Globicephala melas, are slaughtered. DNA fingerprinting using tissue samples from individuals and fetuses showed that female pod members were closely related, and that offspring were probably sired by males from other pods (Amos et al. 1991). Using microsatellite loci, the authors showed that males neither dispersed from, nor bred in, their natal pod (Amos et al. 1993a). So it seems likely that mating occurs when pods meet and temporarily fuse.