The Advances of Genetic Markers and their effect on the future of understanding behavioural ecology: Mating Systems and Social Grouping
Molecular tools that assess kinship within and among populations has allowed for the discovery of unknown mechanisms present in social groupings and behavioural ecology. Monogamy, once thought to be prevalent within certain communities, has been rejected with the discovery of extra-pair fertilizations (EPF) and floater males. As well, conspecific brood parasitism (CBP) has been discovered, advancing the ideas of kin recognition and altruism within social groupings. The ability to assess kinship within social groups has allowed for the discovery of non-reproductive helpers, showing that indirect fitness is a crucial factor in an individual's reproductive success. Dispersal is a behavioural mechanism that is being shown to reduce the ability for inbreeding to occur within family groupings. Therefore, with the use of molecular tools, the ability to assess kinship within groups has allowed for the discovery of many mechanisms that were formally unknown within social group dynamics.
Behavioural Ecology is the study of the evolutionary and ecological basis for behaviour, how behavior allows an individual to adapt to its surrounding environment (Krebs and Davies 1977). Social behavior describes mating behaviours of individuals, as well as family and group interactions. This includes aspects of cooperation and competition, behaviours that influence the evolution of structured society. Initially, in the field of behavioural ecology, Fisher and Haldane largely focused on quantifying natural selection (Haldane 1954, Fisher 1930). Predictions surrounding the behaviours of individuals centred on the idea that behaviour must have evolved because they increase the fitness of the individual. This is the central idea of natural selection, which explains that reproductive fitness of an individual will be selected by environmental conditions. However, molecular tools have allowed for the broadening of these ideas, with the ability to make social and behavioural connections based on quantitative data (Parker et al. 1998). The use of amplified fragment length polymorphism (AFLP), amplification of restriction enzyme cuts of DNA, and microsatellites, tandem base repeats, can show relation between individuals of a population because they have a high mutation rate. A high mutation rate, using fragments of DNA that are not under selection, has more precision when examining individuals; however, they are unfavourable when doing among population analyses. For instance, the emergence of molecular tools has resuscitated the study of mating systems, including monogamy, by showing that monogamy and sexual exclusivity are not exchangeable (Fietz et al. 2000). Other forms of mating systems have also been studied using molecular tools, providing insight into population mechanisms not well known by researchers. The use of molecular tools has also granted insight into social structures, focusing on the reproductive success of individuals within their social group. This includes kin social groups, and the effect of kin selection on the breeding success of individuals, in terms of acquiring dominance within the group and the existence of non-breeding helpers to increase indirect fitness of an individual. This review will outline the advancements in the understanding of diverse mating systems and social groups in nature, using overviews of recent publications that have utilized genetic tools of kinship in the study of behavioural ecology.
How individuals obtain mates and how long the mates stay together are two questions addressed when studying mating systems of populations. Mating systems can be defined as monogamous, having only one sexual partner during the breeding season, or polygamous, which involves having more than one mating partner during a breeding season. In a population of Arctic Ground squirrels, the female is polyandrous, acquiring many male mates throughout the breeding season. DNA fingerprinting analysis revealed that although many mates are acquired by the female during the breeding period, over 90% of the pups are sired by the first mate (Lacey et al. 1997). Therefore, this grants insight into the competitive nature of populations, where males not only have to compete for the female's attention, but also compete amongst gametes for reproductive success. Gamete competition alters the behaviour of the males in the population, especially in context of mate choice, because a male would prefer a virgin female to solidify direct reproductive success. How males compete for access to those females, and how they behave in order to achieve fertilization success are other behaviours of the male individuals that are affected.
Monogamy: Does partner monogamy mean offspring genetic monogamy?
Of particular interest are the unexpected results collected when investigating monogamous relationships in nature. High Extra-Pair Fertilization (EPF) has been found, through genetic markers, in many mating systems where monogamous pair-bonds are formed. Social monogamy is not necessarily indicative of paternal monogamy, with EPFs leading to multiple paternities in litters, including the Australian sleep lizard, Tiliqua rugosa (Bull et al. 1998). Other populations that demonstrate EPFs include the hooded warbler (Wilsonia citrina) and lesser snow geese (Stutchbury et al. 1997, Lank et al. 1989). Even within populations that form pair-bonds, incidences of 'floater males who do not form pairings, copulate successfully with the female population. Minisatellite DNA profiling showed that about half of the EPFs of the stitchbird (Notiomystis cincta) were fathered by unpaired males (Ewen et al. 1999). Two unpaired males were found to have successful fertilizations than on male who was paired with two reproductive females. This demonstrates that being an unpaired male is a strategically successful mating strategy, especially in a male dominated population, where high competition exists and access to females are limited.
Conspecific Brood Parasitism (CBP) is another subset of mating systems confirmed by molecular analysis. CBP occurs when females lay their eggs in the nest of other conspecifics, and has been found to be prevalent in over 200 species of birds, including the House Sparrow, Passer domesticus, and American coots, Fulica americana (Kendra et al. 1988, Lyon 1993). A problem associated with testing whether a clutch of eggs has been parasitized is that a DNA sample of all individuals of interest is required. This can be hampered by incidence of nest failure, or reduced hatching success as a result of unsynchronized breeding cycles between the host and the parasitic egg. Also, destruction of parasitic eggs by the host does occur, therefore protein fingerprints used. They are derived by acquiring an egg albumin sample, a noninvasive process. Incidence of CBP was documented in goldeneye, Bucephala clangula, and it was found that the host may gain inclusive fitness by preferentially accepting the eggs of close relatives. This act of kin selection would eliminate the cost of parental care for the relative. Kin selection may be achieved indirectly by a combination of philopatry, which is the behaviour of returning to your birthplace, recognition of birth rates, or directly by sophisticated kin recognition (Andersson & Ahlund 2000). Hudson's Bay populations of common eider, Somateria molissima sedentaria, also partake in CBP (Andersson & Waldeck 2007). Another potential mechanism leading to host-parasite relatedness, and therefore kin selection, is the similarities in seasonal timing of egg-laying between related individuals. The likelihood of parasitism increases with kin synchronization in Snow Geese, and would reduce the probability of a sophisticated kin recognition mechanism (Findlay & Cooke 1982). CBS may also be the indirect consequence of long-lasting social interaction with kin leading to a shared environment and resources.
Family Groups: The importance of kin selection
When a collection of relatives live in a social group, there is an opportunity for an individual to help increase the reproductive success of kin. The inclusive fitness of an individual is the sum of their direct fitness, or own reproductive success, and indirect fitness, the reproductive success of their kin (Hamilton 1964). Essentially, this takes into account the total lifetime effect on the gene pool of succeeding generations, both through the production of one's own offspring, and through the effects on the reproduction of other individuals. Natural selection depends on the likelihood that the offspring genetically resemble the parents. A subclass of natural selection is kin selection, which depends on the likelihood that relatives genetically resemble one another. Therefore, by increasing the reproductive success of close relatives, you are indirectly increasing the frequency of one's own alleles in the population. Hamilton (1964) outlined variables that affect the likelihood of altruistic behaviour between individuals, including, first and foremost the genetic relatedness of the individuals. Therefore, the more closely related the individuals, the more likely that an act of altruism will occur. As well, the magnitude of benefit to the aided individual is taken into consideration. The greater the benefit of the aid on the individual, and consequently the individual's reproductive success, the more likely it will be given. Lastly, the magnitude of the cost to the altruist in terms of their consequential loss of fitness is taken into consideration before an altruistic act occurs (Hamilton 1964). Examples of altruistic acts include alarm calls, like trills in ground squirrels that function to warn relatives of dangers, and sterile workers in honeybees (Apismellifera) that act to increase the reproductive success of the queens (Sherman 1977, Evans & Wheeler 1999). Molecular markers allow the quantitative studies of social groups, exact distribution of reproduction, and genetic relatedness among members of a group that were previously gathered from qualitative behavioural and demographic data.
Alliance formation between reproductive males secures mating access to females, and allow for effective defending of their mutual territory. This has been described for many mammalian species, including cheetahs and lions (Packer et al. 1988). Wild chimpanzees, Pan troglodytes, maintain cooperative alliances, occasionally participating in cooperative boundary patrols and frequently sharing meet between individuals in the group (Matini et al. 2000). Male bottlenose dolphins, Tursiops truncatus, in the Bahamas were also found to form alliances with kin. Using mtDNA and microsatellite DNA markers, relatedness between the male bottlenose dolphins was found to be significantly correlated with the strength of association between pairs of males. Benefits of cooperation between related individuals can be directly beneficial, with alliances leading to strong reproductive success, or indirectly, through inclusive fitness resulting from enhanced reproductive success of kin (Parsons et al. 2003). Social groups in African lions have also been investigated using DNA fingerprinting and minisatellite banding. Incoming males kill or evict the dependent young of the prior coalition, thereby destroying the genetic input from other males, and increasing the concentration of their alleles within the population. The genetic tools discovered that female companions within a pride are always closely related, and that the males are either closely related or unrelated (Packer et. al 1991). It was found that in larger prides, kinship is essential in maintenance of larger populations where reproduction is highly skewed to favour a few individual males. However, in small populations, where the probability of breeding is usually high, kinship is unnecessary in reproductive success. In the larger prides, where kinship is necessary, there is usually a non-breeding helper male. The presence of this non-breeder acts to increase the reproductive success of their companions by defending their ability to access the female mates. They have no personal reductive success; therefore their genetic representation in subsequent generation occurs through the increasing reproductive success of closely related individuals. This is a large act of kin altruism, where the altruist sacrifices their own personal fitness for the fitness of others.
Social structure acts to prevent loss of genetic variation. Relatedness has been found within packs of African wild dogs (Lycaon pictus) with the use of microsatellites (Girman et al. 1997). Increased hunting success, along with the mutual defence of territory, were benefits of living in packs. It was found that as the patterns of relatedness increased, so did the correlation between the timing of dispersal and the destination of dispersal. Long-distance migration allows for the infusion of genetic diversity. As well, maintenance of a structured pack that inhibits inbreeding allows for the retention of high genetic variability. Inbreeding within a population acts to reduce the amount of heterozygosity, variation in alleles, thereby reducing the genetic variation within the population. With a reduction in genetic variability, populations are more susceptible to extinction. Molecular markers have allowed for the investigation into wild populations, granting insight into the behavioural mechanisms that act to prevent inbreeding. Gray wolves (Canis lupus) commonly live in packs, which would seem to increase the probability of breeding occurring between related individuals. However, the use of microsatellites found inbreeding to be uncommon (Smith et al. 1997). Therefore, a behavioural adaptation to avoid inbreeding within wolf packs has been found to be dispersal. Frequent pairings of unrelated wolves ensures genetic heterogeneity within wolf packs.
Does Dominance in a Social Group mean High Breeding Success?
It has been assumed that individuals within a population compete for dominance because it is correlated with a high reproductive success rate. Parentage assignment using molecular markers has confirmed this hypothesis in many species, but has rejected it in others. A high correlation between dominance and reproductive success has been inferred from behavioural observation in Savannah baboons, Patio cyanocephalus, along with the use of DNA fingerprinting (Altmann et al. 1996). As well, DNA fingerprinting analyses on mandril (Mandrillus sphinx) infants born over five successive years showed that all of them were fathered by only two dominant males (Dixson et al. 1993).
Nonfamily Social Group Structure: Is kin selection necessary?
Kin selection is not the only factor that can explain social behavior. Living in groups reduces predation and increases resource acquisition, whether kin related or not. However, competition may be prevalent in such groupings, where kin selection does not exist. Therefore, this diminishes the importance of the reproductive success of others in the same group. Molecular markers can be used to identify whether the group consists of kin, or of unrelated individuals. Then, the competition for mates can be assessed through the use of molecular markers to determine whether there is a high probability of extra-pair matings. Non-family groupings were found through the use of allozyme electrophoresis in vampire bats, Dasmodus rotundus, who roost together in female associations. This allows for sharing of food resources (blood) between individuals, reducing the cost per individual of energy expenditure (Wilkinson 1985). However, the use of allozymes, different allelic forms of nuclear-coded enzymes, provides limited insight into individual identification in most systems because they possess too few polymorphisms (few variants encoded by a single locus).
The advancements in genetic markers for kin recognition has challenged previous views on the behavioural social structure of populations, and allowed for the formulation of new hypotheses. More variation has been found to exist within and among populations than previously recognized, and with the development of new, more precise and cost effective techniques, more advancements will be made in regards to understanding the social structures of populations that have been previously unknown. Independent assessments will be made in regards to social bonds versus sexual mating. The idea of monogamy has now been challenged, and is proven to be less simple than previously thought. The use of molecular techniques has the ability to investigate among population bonds, as well, among species bonds. Phylogeographic data derived from molecular techniques have the capacity to discover the migration and speciation of populations over geographic time scale. Most of the data that has been collected regarding social behaviour has used genomic regions that are highly variable and are not under selection. However, in the future, the possibility of using particular loci that are functional will provide knowledge about how these expressed loci influence the behaviour of organisms (Hughes 1998).