The Expression of the 2D:4D ratio across the Order Primates

The ultimate causes of variation in primate behaviour and social systems have been well studied, but less attention has been paid to the underlying role of proximate mechanisms. Using the second-to-fourth digit ratio (2D:4D ratio) as a biomarker for prenatal androgen effects (PAE) and phylogenetic comparative methods where appropriate, this thesis aims to complement the ultimate perspective by assessing the degree to which variation in PAE may provide a proximate explanation for the observed variation in primate behaviour. Specifically, this study examines 1) the role of PAE in male intrasexual competition and mating behaviour in non-human primates, 2) the relationship between PAE and human marriage systems, 3) the role of PAE in female intrasexual competition and social relationships in non-human primates and 4) the role of PAE in the expression of aspects of human and non-human primate personality.

In study 1, a cross-species analysis investigating the relationship between PAE and aspects of intrasexual competition in male non-human primates revealed no relationships between 2D:4D ratios and anatomical traits associated with male intrasexual competition (male canine crown height and canine crown height dimorphism) or male reproductive skew and mating skew. Male digit ratios did, however, vary across species characterised by different types of mating systems; males of species characterised by monogamous mating had the highest 2D:4D ratios, followed closely by polyandrous males (low inferred PAE), while polygynandrous and polygynous males had the lowest 2D:4D ratios (high inferred PAE). Male 2D:4D ratios also varied with the form of polygyny and polygynandry corresponding to the need for males to display competitive over cooperative behaviours in each mating system. Higher PAE may therefore be adaptive for male non-human primates which experience high levels of direct intrasexual competition. This pattern was also evident in female non-human primates (Study 3), but was not mirrored in analysis of humans, where no associations were found between male or female 2D:4D ratios and marriage system (Study 2). As males are the competing sex among humans, there is likely strong selective pressure for high PAE regardless of the marriage system. Likewise, due to its negative impact on female fertility, sexual selection may favour low PAE in human females regardless of the marriage system. However, as the sample was biased in favour of monogamous populations, a more balanced dataset encompassing a wider range of marriage systems may provide further insights.

PAE were also implicated in the maintenance of intersexual dominance relationships, particularly female dominance, as evidenced by lower female 2D:4D ratios in species characterised by female dominance than in species characterised by male dominance or codominance (Study 3). There was no evidence that variation in female-female dominance interactions is associated with variation in PAE across the primate order as evidenced by the lack of relationships between 2D:4D ratio and rates of female-female agonism or the directional consistency of agonistic interactions among females (argued to be a measure of the extent to which dominance relationships are despotic vs egalitarian), although these analyses were based on small sample sizes. Likewise, relationships between 2D:4D ratios and degree of frugivory and group size were nonsignificant, possibly because these variables are not good measures of direct intrasexual competition among females. However, in a more taxonomically-narrow analysis conducted with macaque species (Macaca spp.), female 2D:4D ratio varied according to social style, with more "tolerant" species having higher 2D:4D ratios than less tolerant species, suggesting that PAE may contribute to this variation. Results indicate that PAE may act as a proximate mechanism underlying behavioural expression in male and female non-human primates in ways that are ultimately adaptive to their social system.

In study 4, PAE on behavioural variation within species was explored using personality traits (boldness, exploration tendency/curiousness, persistency, competitiveness) in three species: ring-tailed lemurs (Lemur catta), robust capuchins (Sapajus spp.) and human children (Homo sapiens). 2D:4D ratios were not associated with any trait in ring-tailed lemurs or with persistency in any species, suggesting that expression of this trait may not be influenced by PAE. Boldness and exploration tendency in boys correlated negatively with 2D:4D ratios, as did competitiveness in robust capuchins, suggesting that PAE play a role in the expression of these traits in these and perhaps also in other haplorhine primates. In addition to broad cross-species influences, PAE thus appear to underlie inter-individual differences in the expression of some adaptive behavioural traits, highlighting the importance of considering proximate as well as ultimate causes in studies of primate behaviour.