Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals

Abstract

Pheromones are chemicals emitted and sensed by conspecifics to elicit social and sexual responses and are perceived in terrestrial vertebrates primarily by the vomeronasal organ (VNO). Pheromone receptors in the mammalian VNO are encoded by the V1R and V2R gene superfamilies. The V1R superfamily contains 187 and 102 putatively functional genes in the mouse and rat, respectively. To investigate whether this large repertoire size is typical among mammals with functional VNOs, we here describe the V1R repertoires of dog, cow, and opossum based on their draft genome sequences. The dog and cow have only 8 and 32 intact V1R genes, respectively. Thus, the intact V1R repertoire size varies by at least 23-fold among placental mammals with functional VNOs. To our knowledge, this size ratio represents the greatest among-species variation in gene family size of all mammalian gene families. Phylogenetic analysis of placental V1R genes suggests multiple losses of ancestral genes in carnivores and artiodactyls and gains of many new genes by gene duplication in rodents, manifesting massive gene births and deaths. We also identify 49 intact opossum V1R genes and discover independent expansions of the repertoire in placentals and marsupials. We further show a concordance between the V1R repertoire size and the complexity of VNO morphology, suggesting that the latter could indicate the sophistication of pheromone communications within species. In sum, our results demonstrate tremendous diversity and rapid evolution of mammalian V1R gene inventories and caution the generalization of VNO biology from rodents to all mammals. evolution ͉ dog ͉ cow ͉ opossum ͉ rodents

Extraordinary Diversity of Chemosensory Receptor Gene Repertoires Among Vertebrates

“…1b ). The phylogenetic analysis revealed at least From Shi and Zhang (2007) e From Young and Trask (2007) f From Shi and Zhang (2006) h From Zhang et al (2007) i From Grus et al (2005) j From Niimura and Nei (2005) k From Niimura and Nei (2006) l From Alioto and Ngai (2005) m From n From Saraiva and Korsching (2007) nine ancestral OR genes (or gene lineages) in the most recent common ancestor (MRCA) of fishes and tetrapods (Niimura and Nei 2005) (Fig. 1b ).…”

“…However, the functional V1R repertoire is small, with only four open reading frames in most individuals Zhang and Webb 2003) . Grus et al (2005) identified functional V1R genes from five orders of placental and marsupial mammals ( Table 1 ). The intact V1R repertoire size varies by at least 23-fold among mammals with functional VNOs and this size ratio represents the greatest among-species variation in gene family size of all A more recent study found that the platypus, a semiaquatic monotreme, has the largest V1R repertoire characterized to date, with 270 potentially functional genes and 579 pseudogenes.…”

“…In contrast to mammals, fishes have highly conserved V1R-like repertoires, containing four genes in two pufferfish species and five genes in zebrafishes, stickleback, and medaka, respectively (Hashiguchi and Nishida 2006 ;Saraiva and Korsching 2007 ;Shi and Zhang 2007) . Interestingly, the number of intact V1R genes is positively correlated with the morphological complexity of the VNO, suggesting that VNO morphology is a good indicator of vomeronasal sensitivity (Grus et al 2005) .…”

“…In mammals, both gene duplicate and pseudogenization have played important roles in generating the remarkable among-species variation in V1R gene repertoire (Grus et al 2005 ;Young et al 2005) . On one hand, substantial numbers of gene duplication events occurred independently in monotremes, marsupials, and placentals, giving rise to platypus-specific, opossum-specific, and placental-specific gene clusters (Grus et al 2005(Grus et al , 2007 (Fig.…”

“…On one hand, substantial numbers of gene duplication events occurred independently in monotremes, marsupials, and placentals, giving rise to platypus-specific, opossum-specific, and placental-specific gene clusters (Grus et al 2005(Grus et al , 2007 (Fig. 3a ).…”