title: Prenatal androgen effects and social evolution in haplorhine primates: Evidence from the second-to-fourth digit ratio (2D:4D)
Creators: name: Nelson, Emma
Publisher: name: University of Liverpool Repository
Year: 2016

description: Prenatal androgens play a key role in sexual differentiation. In humans and rhesus macaques prenatal androgens have been implicated in variation in the development of sexually selected behaviours and cognitive abilities in both males and females. The primacy of prenatal androgens in organising traits linked to sociality suggests great pertinence to the evolutionary substrate that underpins social behaviours in all higher primates. In humans the second-to-fourth digit ratio (2D:4D) is a marker for prenatal androgen effects. Low 2D:4D has been indirectly linked to higher foetal androgens and high 2D:4D has been indirectly linked to lower foetal androgens. Individuals with low 2D:4D express higher competitiveness, promiscuity and more masculinised social cognitive abilities. Low 2D:4D is also more common in polygynous societies. This thesis uses 2D:4D as an anatomical biomarker with phylogenetic comparative methods to investigate co-variation between prenatal androgen effects and traits linked to sexual selection in haplorhine primates. In the process, measurements were taken of the 2nd and 4th digits of 1286 captive individuals from 74 species. An intra-specific study of 2D:4D and dominance ranks in female rhesus macaques is presented and shows that low 2D:4D is more common in higher ranking females. The result suggests that prenatal androgens may be implicated in supporting dominance ranks across generations. A comparison of digit ratios in mother-infant dyads in the same cohort shows heritability of 2D:4D to be high; values are similar to humans and more distantly related taxa. Moving to inter-specific analyses: results enclosed provide the first robust evidence that 2D:4D generalise across a taxonomic group and striking parallels are shown between cross-species analyses and results from earlier human 2D:4D studies. In particular, evidence is presented that 2D:4D is lower in polygynous species with higher levels of intra-sexual competition and higher in pair-bonded species with lower levels of intra-sexual competition. These studies also show that 2D:4D co-varies with both core behavioural characteristics and androgen profiles in catarrhines: in comparison to the great apes, Old World monkeys exhibited low 2D:4D, higher intra-sexual competition and more reactive androgen profiles. These differences might reflect prenatal androgen effects on programming neuro-psychological pathways that potentiate social behaviours and social bonding patterns according to different levels of sexual selection. Focussing on the great apes; 2D:4D is shown to increase from Pongo sp. to Homo sapiens. It is proposed that this reflects a decrease in prenatal androgens and androgen sensitivity across this clade. That being the case; fossilised digit bone ratios permitted prenatal androgen effects to be traced across extinct apes and hominins. The findings indicate that Miocene apes might have experienced a down-regulation of the androgen response. Reducing masculinisation is also detected across time in Australopithecus afarensis, but not Ardipithecus ramidus. Evidence from Middle and Late Pleistocene hominins indicates that prenatal androgen effects continued to decrease over evolutionary time. The most recent increase in digit ratios appears to have coincided with shifts in social organisation as modern humans entered a new ‘adaptive space’ with the advent of agriculture at the beginning of the Holocene. These changes are consistent with hypotheses proposing a ‘feminisation’ or ‘domestication’ event coinciding with reductions in dominance and competitive behaviours throughout hominin evolution, right up until relatively recent times. Analyses of 2D:4D identify prenatal androgen effects as strong candidates in the evolution of sexually selected behaviours and social bonding in haplorhines. Application of 2D:4D could thereby improve our current understanding of primate social evolution if incorporated within research into the bio-behavioural processes that underpin sociality across taxonomic groups. Finally, because hominin evolution is so strongly associated with the emergence of specialised cognitive adaptations to cope with changes in social organization, 2D:4D could prove to be a window into our own past.