Converging roles of glutamate receptors in domestication and prosociality

Abstract

8The present paper highlights the prevalence of signals of positive selec-9 tion on genes coding for glutamate receptors-most notably kainate and 10 metabotropic receptors-in domesticated animals and anatomically mod-11 ern humans. Relying on their expression in the central nervous system 12 and phenotypes associated with mutations in these genes, we claim that 13 regulatory changes in kainate and metabotropic receptor genes have led 14 to alterations in limbic function and Hypothalamic-Pituitary-Adrenal axis 15 regulation, with potential implications for the emergence of unique social 16 behaviors and communicative abilities in (self-)domesticated species. 17 1 Introduction 18 Under one account of recent human evolution, selective pressures on prosocial 19behaviors led not only to a species-wide reduction in reactive aggression and the 20 extension of our social interactions [1, 2], but also left discernible physical mark-21 ers on the modern human phenotype, including our characteristically "gracile" 22 anatomy [3, 4]. 23 It has long been noted that these morphological differences resemble those 24 of domesticated species when compared with their wild counterparts [5]. Ex-25 perimental observation of domestication unfolding in wild farm-bred silver foxes 26 has unequivocally shown that selection for tameness alone can affect develop-27 mental trajectories to bring about a suite of physiological and behavioral traits 28 indicative of the "domestication syndrome" [6]. This raises the possibility that 29 morphological changes in Homo sapiens resulted from selective pressures on 30 reduced reactivity to encounters with conspecifics. In turn, this predicts over-31 lapping regions of selection and convergent physiological effects in the genomes 32 of domesticated species and modern humans.33In a recent comparative study, we have shown that genes with signals of 34 positive selection pooled across different domesticated species -dog, cattle, 35 cat, and horse -have above-chance overlap with genes exhibiting signals of 36 selection in AMH, suggestive of convergent evolutionary processes [4]. Signals 37 on glutamate receptor genes were identified more consistently than any other 38 gene class across human and domesticate selective-sweep studies, and will be 39 the focus of this paper. 40Glutamate is the primary excitatory neurotransmitter in the vertebrate ner-41 vous system, essential for fast synaptic transmission and plasticity, learning, 42 memory, and modulation of Hypothalamic-Pituitary-Adrenal (HPA) activity. 43 [7]. The 26 glutamate receptors are primarily localized at synaptic nerve ter-44 minals in the brain and are divisible into two broad families (ionotropic and 45 metabotropic). There are various widely used names for each receptor and 46 corresponding gene in the literature. For ease of reference, see Table 1. 47 84 accessory subunit, and related G-protein signaling cascade genes. We review 85 some of the most noteworthy of these in Supplementary Section S1. 86At least one glutamate receptor gene shows...

Epimutations in Developmental Genes Underlie the Onset of Domestication in Farmed European Sea Bass

“…Members of the glutamate receptor family deserve particular attention because they have been found under positive selection in the genomes of all domesticated species studied without exception (O’Rourke and Boeckx 2018), and including the sea bass after 25 years of selective breeding (Bertolini et al. 2016) (supplementary fig.…”

“…2 and supplementary data set 1, Supplementary Material online). We found several genes in common, among them genes coding for glutamate receptors, which are found under positive selection in all the domesticates examined (O’Rourke and Boeckx 2018). This, along with the observation that farmed sea bass also shares some of the characteristics of the domestication syndrome, for example, changes in morphology (Arechavala-Lopez et al.…”

Oxytocin and vasotocin receptor variation sheds light into the evolution of human prosociality

“…Still, our results, especially those concerning the AVP receptors, also point to a distinct MHS social profile, which meshes well with the predictions of another working hypothesis that tries to account for modern humans’ prosociality, the ‘selfdomestication hypothesis’. Advocates of this hypothesi 14, 15, 101 , build their case on certain physiological and behavioral traits that modern humans share with domesticated animals to argue for a significant turning point exclusive of Homo sapiens on the prosocial continuum. Although he does not endorse the logic of self-domestication, 6 also recognizes a special transition corresponding to the emergence of our species.…”

Social modularity: conserved genes and regulatory elements underlie caste-antecedent behavioural states in an incipiently social bee

“…Glutamate and its receptors have been found to play a key role in task specialization within divisions of labour in other social insects (e.g. C. australensis [18]; A. mellifera [59]; leaf-cutting ants, Atta vollenweideri [60]), and in the adoption and/or expression of social traits among vertebrates (including mice [61], dogs and humans [62]). Glutamate-related genes thus represent a particularly promising deeply conserved candidate suite for further functional and comparative genomic investigations into the emergence and elaboration of sociality [15,16].…”