Comparative Genomic Analysis of the Pheromone Receptor Class 1 Family (V1R) Reveals Extreme Complexity in Mouse Lemurs (Genus, Microcebus) and a Chromosomal Hotspot across Mammals

Abstract

Sensory gene families are of special interest for both what they can tell us about molecular evolution and what they imply as mediators of social communication. The vomeronasal type-1 receptors (V1Rs) have often been hypothesized as playing a fundamental role in driving or maintaining species boundaries given their likely function as mediators of intraspecific mate choice, particularly in nocturnal mammals. Here, we employ a comparative genomic approach for revealing patterns of V1R evolution within primates, with a special focus on the small-bodied nocturnal mouse and dwarf lemurs of Madagascar (genera Microcebus and Cheirogaleus, respectively). By doubling the existing genomic resources for strepsirrhine primates (i.e. the lemurs and lorises), we find that the highly speciose and morphologically cryptic mouse lemurs have experienced an elaborate proliferation of V1Rs that we argue is functionally related to their capacity for rapid lineage diversification. Contrary to a previous study that found equivalent degrees of V1R diversity in diurnal and nocturnal lemurs, our study finds a strong correlation between nocturnality and V1R elaboration, with nocturnal lemurs showing elaborate V1R repertoires and diurnal lemurs showing less diverse repertoires. Recognized subfamilies among V1Rs show unique signatures of diversifying positive selection, as might be expected if they have each evolved to respond to specific stimuli. Furthermore, a detailed syntenic comparison of mouse lemurs with mouse (genus Mus) and other mammalian outgroups shows that orthologous mammalian subfamilies, predicted to be of ancient origin, tend to cluster in a densely populated region across syntenic chromosomes that we refer to as a V1R “hotspot.”

Platypus and echidna genomes reveal mammalian biology and evolution

“…Therefore, the diversification of the olfactory bulb and accessory olfactory bulb systems in monotremes provide an interesting example of the eco-evolutionary trade-off. V1R amplification has been associated with the size of the vomeronasal organ and nocturnal activity 30 . This is also consistent with the fact that the platypus closes its eyes when diving and therefore relies entirely on other senses underwater and in the burrow.…”

Distinct evolutionary trajectories of V1R clades across mouse species

“…This pattern of gene birth-and-death results in lineage-specific receptor repertoires [19]. Consequently, there are substantial differences in receptor sequences and repertoire size across divergent species [22][23][24][25][26][27][28][29]. For example, among three mammalian species (dog, opossum, and house mouse) there are virtually no one-to-one VR orthologs [19].…”

The evolution of sexual signaling is linked to odorant receptor tuning in perfume-collecting orchid bees

“…In addition, several gene families involved in the sensory perception of chemical signals have been shown to mirror these evolutionary dynamics 4,8,9 . For example, olfactory receptor genes tend to differentiate rapidly in disparate groups of animals including lemurs 10 , rodents 11 , and moths 12 . However, it remains unclear how sexual chemical signaling evolves in a genome-wide context and contributes to the early diversification of species.…”