It has been argued that inbreeding, the mating of related individuals, represents a significant threat to the health and viability of individuals and populations. The potentially deleterious effects of mating with one’s kin are legion, including: Increased infant mortality (Packer 1979; Ralls and Balou 1982; Smith 1995); increased risk of cancers (Crawford and O'Rourke 1978); increased rates of spontaneous abortion (Smith 1995b); abusive behaviour towards offspring (Jones 1995); low birth weight (Wildt et al 1982) and lower resistance to infection (O'Brien and Evermann 1988). The primary basis of these effects, termed inbreeding depression, is genetic. The reason for this is that alleles for deleterious effects are usually recessive (Moore and Ali, 1984). Thus it is more likely that two copies of a recessive allele will be passed to an infant when two relatives mate than if two random individuals breed. The reason for this is that related individuals may share copies of alleles by common descent.
The degree of consanguinity necessary before inbreeding depression is seen can vary between species. This statement is based on the premise that inbreeding, with resultant inbreeding depression, will act to eliminate many deleterious alleles from the gene pool, thus necessitating a closer relationship between mated individuals before any effect will be seen (Ralls and Balou 1988). Smith (1995a) discussed this proposition in the context of an inbred colony of rhesus macaques (Macaca mulatta). The coefficient of relatedness, given the symbol r, is a measure of how likely two individuals are to share alleles via common descent. Smith showed that where individuals had a co-efficient of relatedness of less than 0.125 no depression was seen; an r-value of 0.125 corresponds to two half-siblings. This level was much greater than other species he examined, leading Smith to suggest that M.mulatta was especially inbred at some point in its evolutionary history.
The preceding evidence seems to suggest that inbreeding is something to be avoided wherever possible, a process that can be undertaken in two ways:
with their relatives. (Itani, 1972) and/or
Sex-biased dispersal is extremely common, with males dispersing at sexual maturity while females remain philopatric in a wide range of species (Clutton-Brock and Harvey, 1976; Greenwood, 1980). An "incest taboo", as the second method is often termed (Imanishi 1966), is subtle and more difficult to detect. Nevertheless researchers have found that a strong inhibition, preventing mating between maternal kin, is common, being found in some primates: Papio cynocephalus hamadryas (Kummer, 1968; Alberts and Altmann, 1995); Papio cynocephalus anubis (Packer, 1979); Macaca fuscata; Perry and Manson 1995); Macaca sylvanus (Paul and Kuester, 1985); M.mulatta (Missakian 1973; Smith 1995b) Cercopithecus aethiops (Clutton-Brock, 1988). Interestingly Paul and Kuester (1994) found that paternally related M. sylvanus would happily breed with one another, a similar picture to that seen in the M.mulatta studied by Smith (1995b). This inhibition maybe based on familiarity rather than intrinsic knowledge of relatedness between individuals. Paul and Kuester (1994) found that female M.sylvanus strongly avoided mating with unrelated males who acted as alloparents for them during their infancy, suggesting that familiarity early in life is a key to avoidance. Perloe (1992) found a similar pattern in a M.fuscata group, the alpha and beta males never mated over two mating seasons. The author suggests that these two males were victims of their own success, having dominated the group for an unusually long time thus they were familiar to all the sexually active females without having actually sired any of them.
Over the years a debate has raged as to the ultimate cause of this sexually biased dispersal pattern amongst mammals, and especially amongst the primates. Given the wealth of populations and captive colonies available for study, the focus fell upon the Cercopithcines. Specifically those living in a polygynous mating system, the macaques, baboons and a solitary species of Cercopithecus, the vervet monkey C.aethiops. In order for Itani's (1972) theory of inbreeding avoidance to hold, it would be necessary to show a cost to non-dispersal, Craig Packer achieved this in 1979.
In January of that year he reported the result of a study of the less famous residents of Tanzania's Gombe National Park, the olive baboons (P.anubis). Whilst examining male dispersal patterns Packer observed that several years earlier a male, Bramble, was born into B troop. As he grew so did his troop until it eventually fissioned, giving A and B troops. Bramble eventually left B troop, as is normal for his species at about 7 years old, the troop he migrated into however, was A troop, one containing significantly more related individuals than if he had joined another group. Packer examined the survivorship of infants to one month old of infants sired by Bramble compared to those sired by other males. This period was chosen as the infant was still dependent on its mother and thus less likely to meet an accidental death. Also, any congenital problems were likely to take their effect within this time. First Packer found that, when excluding Bramble from the analysis, infant mortality to one month was uniform across all groups. On including Bramble, a huge difference was found. Amongst infants sired by males other than Bramble, all but 15.8% survived to one month of age while only 50% of Brambles sires did. This was pointed to as quantitative evidence of inbreeding depression in a wild population; in 1982 Ralls and Ballou followed this with their paper showing that inbreeding increased infant mortality to one month old in Macaca fascicularis and Macaca nigra.
Moore and Ali (1984) argued that male natal dispersal was a result of intra-sexual competition and that any associated avoidance of inbreeding was, at best, coincidental. This position was based on Wade's (1979) discussion of kin selection amongst baboon species, arguing that inbreeding increases the r value of individuals in a group, making one more able to benefit from kin selection, and promoting altruistic sociality. The logical basis of this argument, Hamilton's 1966 theory of kin-selection creating "beneficial inbreeding" (Moore and Ali, 1984, p95). However, Moore and Ali argue for costly outbreeding, stating that it decreases homozygosity, dilutes genotypes that are adapted to the local environment, incuring the costs associated with dispersal (i.e. increased predation risk, reduced foraging efficiency). Moore and Ali's adoption of intra-sexual competition as the ultimate cause of male dispersal was, they felt, supported by the aggression directed towards males of an emigrant age (adolescents) by older males.
Packer (1984) rebuffed this argument, pointing out that although adolescent males did receive considerable aggression from older males prior to emigration, they faced far greater aggression from the males of any group they tried to join. This being the case, and allowing for the costs of dispersal, Packer (1984) contended that there must be some major benefit to dispersal with which to offset this aggression as well as the other costs of dispersal mentioned above . Paul and Kuester (1999) were able to show just what this benefit was. Examining a captive colony of M.sylvanus at Affenberg, it was shown that a male leaving a group containing a high number of female relatives would happily join a group containing a higher number of males than his original group. This behaviour would incur higher intra-sexual competition yet inbreeding would be avoided. Further, Paul and Kuester (1999) showed that the decision to emigrate was not based solely on the ratio of females to males. In fact group choice was a function of the ratio of unrelated females to males. By the mid 1980's Itani's (1972) inbreeding avoidance hypothesis had been largely accepted as the ultimate cause of male natal dispersal (but see Moore 1995 for an opposing view).
Debate continued as to the cause of secondary dispersal, a phenomenon again largely associated with males (Greenwood 1980) that being dispersal from a non-natal group. Largely it was felt that males would leave if another group with a higher female to male ratio was available (Packer, 1984). This was the dominant view until 1988 when Tim Clutton-Brock surveyed 19 different species across a range of mammalian taxa. Clutton-Brock found, in all but one case, that the tenure of a male within a group was less than the age at which females of the species attained sexual maturity. The significance of these findings is that a father will be out of a group before his daughters are old enough to breed. A very effective way of avoiding father-daughter inbreeding. Clutton-Brock's findings have since been re-inforced. Alberts and Altmann's (1995) study of the migratory habits of the P.cyncocephalus of Amboseli showed a peak of secondary dispersal in the first year and a longer peak between the sixth and eighth years of residence. The authors found the initial peak to be caused by young males who did not immigrate successfully and were soon ejected. The second peak however, coincides with the onset of sexual maturity amongst females, and thus inbreeding is avoided. These findings combined with those of Packer (1979) and others such as Ralls and Balou (1984); Smith (1995a); Melnick et al (1984); Crawford and O’Rourke (1978) and Paul and Kuester (1994), all of whom demonstraed a cost to inbreeding pointed to inbreeding avoidance as the ultimate cause of male dispersal, both natal and secondary.
Numerous other factors have been found that affect the timing of natal and secondary dispersal, the choice of group emigrated to and so on. Sprague (1992) found that male M.fuscata chose their new group on the basis of sex ratio and of their likely position in the new group . Provisioning has been seen to delay both natal and secondary dispersal, in both Tibetan macaques (M.thibetana Zhao, 1994) and Japanese macaques (M.fuscata, Sprague 1992) the food providing an increased cost to dispersal. Despite this males still left, merely doing so later than normal. A finding suggestive of inbreeding avoidance being a strong impetus to emigration. Moving to the baboons E.O.Smith (1992) found that P. Anubis and P.hamadryas chose their new groups on the basis of the number of same age males within the group, seeking to minimise competition. Alberts and Altmann (1995) examined P.cyncocephalus migration in great detail, they found that males dispersed from the natal group sooner if their mother was old, or if the mother died. This is a similar pattern to that seen in C.aethiops (Cheney 1983). Most intriguingly they found that the sons of high-ranking mothers emigrated significantly sooner than males born to low ranked females. Their explanation of this rests on Altmann et al's 1988 observation that high-ranking P.cynocephalus mothers produced more daughters than sons and vice versa for low ranking females. This being the case high ranking sons will have a lower unrelated female to male ratio and leave sooner than low ranking males who will have a higher unrelated sex ratio and can stay longer and exploit this. However, if one considers that Horrocks (1986) found male natal dispersal of C. aethiops to be subject to a weight threshold, and that Rasmussen (1981) found a strong correlation between body size and age at dispersal for male P. cynocephalus an alternative explanation presents itself. Given that high-ranking mothers are accepted to have access to higher quantities and often quality of food it is logical to predict that their offspring will reach a weight or a size at which they can successfully leave their group sooner than individuals raised on lower quality food.
An interesting aspect of group choice was highlighted by Zhao (1994). His M.thibetana males tended to join neighbouring groups to which other group members had previously emigrated, a phenomenon seen in other species (C.aethiops: Cheney and Seyfarth 1983; Cheney 1981. for review see Melnick and Pearl 1988). Nozawa et al (1982) found that M.fuscata dispersal tended to be within a selection of groups, termed a local concentration of groups. This was effectively a circle of 100 km radius, thus groups over 100 km apart exchanged individuals extremely rarely. A similar picture is seen in M.fascicularis (Kawamoto et al 1984). How then do these species remain outbred if they exchange males only between neighbouring groups? Cheney and Seyfarth (1983) discuss this problem as it relates to the Amboseli vervet population, arguing that this localised dispersal need not be problematic. This, they claim, will be the case if occasionally individuals emigrate alone and at random. In contrast to these studies Melnick et al's 1984 study of wild Indian M.mulatta found that natal dispersal was a random procedure. Drickamer and Vessey (1973), on the other had, found natal dispersal to be significantly affected by sex ratio. This last study was of the provisioned M.mulatta of Cayo Santiago. Boelkins and Wilson (1972) previously pointed out that a comparison between this population and a wild one would not be valid due to the unique nature of the Cayo Santiago population. Kuester et al (1994) found natal dispersal to be tied to the size of ones natal group. The larger one's group the more likely there are to be unrelated females within, thus one can stay longer and not incur the same costs found in a smaller group.
However, despite a strong incest taboo and the "drive" to leave the natal group some individuals do remain in their natal group and breed there. In most reports of this it is impossible to tell whether actual inbreeding has occurred rather than simply mating with an unrelated individual who happens to be in your natal group. Natal mating has been seen in a variety of species, including: P.cynocephalus (Altmann et al 1988); P.anubis (Packer, 1979); P.ursinus (Bulger and Hamilton, 1988); P.hamadryas (Sigg et al 1982); Theropithecus gelada (Dunbar 1984); M.mulatta (Missakian 1973; Chapais 1983; Colvin 1986); M.fuscata (Sugiyama 1976; Huffman 1987); M.sylvanus (Paul and Kuester 1985) and C.aethiops (Cheney et al 1988). The vast majority of these studies were purely observational. Males were seen to mate in their natal group, yet it was all but impossible to find out if they had actually reproduced. Until 1988 paternity could only be assessed by recording matings on the day of peak fertility, a problematic situation given that many female primates are highly promiscuous at this time, immunological assays or blood protein analysis, both of which methods can be very ambiguous given that most primates have low levels of variability in these systems (Inoue et al 1991; Rogers 1992). However, in 1988, Weiss et al utilised the great advances that had been made in DNA extraction and analysis to examine primate paternity. The discovery of minisatellites, regions of DNA containing a variable number of repeated codons by Bell et al (1982) provided the basis for the 1985 creation, by a team lead by Alec Jeffreys, of probes that bound to a common core sequence found in each human minisatellite (Jeffreys 1985). If cut with a restriction enzyme and then run through an electrophoretic gel these probes will deliver the individuals DNA fingerprint, a pattern of bands unique to that individual. Weiss et al (1988) took this human technology and applied it to four Old World monkeys: Macaca silenus; M.fuscata; Erythrocebus patas and Colobus guereza. Human probes were found to hybridise happily with the DNA from these species, thus minisatellites became accepted as a powerful tool in assigning primate paternity. These probes allow researchers to distinguish reproduction from breeding, an important distinction to make given that Missakian (1973) found that adolescent M. mulatta who did not mate with a natal individual would not have any other matings during that year. A similar picture of adolescent incestous sexual behaviour has been recorded in P.anubis (Smuts 1985) and M.radiata (Glick, 1980).
The power of genetic analyses can be seen in the work of Don Melnick and his collaborators. His studies of the microsatellites of the Dunga Gali M.mulatta population (Melnick and Pearl 1996) showed the population to be significantly outbred. This finding is in stark contrast to the behavioural data gathered. Working purely from ethological data it was expected that a degree of inbreeding would be seen, yet it was not. Rapidly minisatellite paternity analysis became incorporated in the investigation of reproductive success in polygynous primates. It had long been assumed that reproductive success was rank dependent. Alpha male produced more offspring than beta males and so on down the hierarchy. In purely behavioural terms this did seem to be the case. Perloe (1992) found the higher a male M.fuscata ranked, the more consortships it had, these consortships lasted longer and occurred closer to the females peak of fertility. A similar pattern was seen in: the Affenberg M.sylvanus population (Paul et al 1993); another M.fuscata group (Inoue et al 1993); M.mulatta (Berard et al 1993); M.arctoides (Bauers and Hearns 1994); M.fascicularis (de Ruiter et al 1994) and P.anubis (Packer 1979).
Weiss et al's (1988) discovery led the way for some very interesting results indeed. Inoue et al (1991; 1992; 1993) used a combination of behavioural observation and minisatellite analysis to assign paternity in a M.fuscata group. As stated above, from observational data the aforementioned dominance-reproductive success relationship was found. Yet, when the DNA data was examined the picture was very different indeed. The number of offspring produced was unrelated to rank. In 1993 Berard et al, working on a small group of the Cayo Santiago M.mulatta found no link between rank and reproductive success. A study of the Affenberg M.sylvanus, performed in 1993 by Paul et al found a similar pattern. Using blood samples taken over a five year period they discovered that of seventy five infants sired by the thirty three sexually mature males of the colony the alpha male did indeed produce the most offspring. However, Paul et al point out that this relationship only exists because of the non-existent reproductive success of the sexually mature, yet not sexually active sub-adult males. This observation fits well with the Bercovitch-McMillan hypothesis, a synthesis of the findings of two papers (Bercovitch 1986; McMillan 1989) both of which found that the inclusion of sub-adult males produced a false-positive relationship between rank and reproductive success. McMillan (1989) explains that the low rank sub-adult males mate far less than fully adult males, even in the absence of any competition, and that their exclusion from analysis removes any rank-reproductive success relationship seen previously. This hypothesis has been confirmed in a number of studies (de Ruiter et al 1992; Paul et al 1993). Bauer and Hearns (1994), however, examined reproductive success in relation to rank in M.arctoides, and after excluding sub-adult males still found a very strong relationship. The alpha male was the only one who sired any offspring over the course of two years of study. This relationship is due to the nature of the reproductive physiology of the species. Females have non-synchronous oestrus, thus allowing the alpha male to enjoy a 100% monopoly on mating during the fertile period of each female. Additionally the females extreme preference for mating with the alpha male and the alpha male alone gives him a huge reproductive advantage.
From the above mentioned studies, questions emerge. Specifically:
1) What does influence natal dispersal? Is it a question of inbreeding avoidance or intra-sexual competition?
2) Why does secondary dispersal occur? Again is it a question of inbreeding avoidance or a matter of declining competitive skills?
3) Why should individuals disperse from their natal groups after the opposite sex have become sexually mature?
4) Are the influences on both forms of dispersal the same in species where the sexual roles are reversed?
The focus of this thesis is the ultimate causeof primary and secondary dispersal amongst polygynous old-world primate species, resolving the inbreeding avoidance Vs intra-sexual competiton debate.