Evolution of threat response-related polymorphisms at the SLC6A4 locus in callitrichid primates

Abstract

Variation in an upstream repetitive region at the SLC6A4 locus, which encodes a serotonin transporter, is associated with anxiety-related behaviour in a few primate species, including humans and rhesus macaques. In this study we investigate evolution of SLC6A4 polymorphisms associated with anxiety-related behaviour in common marmosets (Callithrix jacchus). Assaying variation in the SLC6A4 repeat region across 14 species in 8 genera of callitrichid primates (marmosets and tamarins) we find large interspecific variation in the number of repeats present (24-43). The black tufted-ear marmoset (C. penicillata) has sequence polymorphisms similar to those found in the common marmoset, which is its sister species, and no other species has intraspecific variation at these sites. We conclude that, similar to humans and rhesus macaques, the functional polymorphism at SLC6A4 in common marmosets has a recent evolutionary origin, and that the anxiety-related allele is evolutionarily derived. Common/black tufted-ear marmosets and rhesus macaques share high ecological adaptability and behavioural flexibility that we propose may be related to the maintenance of the polymorphism.