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Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals.

Suárez R, Fernández-Aburto P, Manger PR, Mpodozis J - PLoS ONE (2011)

Bottom Line: We noted that the species that lost the Gαo pathway belong to Laurasiatheria and Primates lineages, both clades with ubiquitous sexual dimorphisms across species.We found that both species show uniform expression of Gαi2-protein throughout AOB glomeruli, while Gαo expression is restricted to main olfactory glomeruli only.Our results suggest that the degeneration of the Gαo-expressing vomeronasal pathway has occurred independently at least four times in Eutheria, possibly related to the emergence of sexual dimorphisms and the ability of detecting the gender of conspecifics at distance.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio de Neurobiología y Biología del Conocer, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Santiago, Chile. rsuarezsaa@gmail.com

ABSTRACT
In mammals, social and sexual behaviours are largely mediated by the vomeronasal system (VNS). The accessory olfactory bulb (AOB) is the first synaptic locus of the VNS and ranges from very large in Caviomorph rodents, small in carnivores and ungulates, to its complete absence in apes, elephants, most bats and aquatic species. Two pathways have been described in the VNS of mammals. In mice, vomeronasal neurons expressing Gαi2 protein project to the rostral portion of the AOB and respond mostly to small volatile molecules, whereas neurons expressing Gαo project to the caudal AOB and respond mostly to large non-volatile molecules. However, the Gαo-expressing pathway is absent in several species (horses, dogs, musk shrews, goats and marmosets) but no hypotheses have been proposed to date to explain the loss of that pathway. We noted that the species that lost the Gαo pathway belong to Laurasiatheria and Primates lineages, both clades with ubiquitous sexual dimorphisms across species. To assess whether similar events of Gαo pathway loss could have occurred convergently in dimorphic species we studied G-protein expression in the AOB of two species that independently evolved sexually dimorphic traits: the California ground squirrel Spermophilus beecheyi (Rodentia; Sciurognathi) and the cape hyrax Procavia capensis (Afrotheria; Hyracoidea). We found that both species show uniform expression of Gαi2-protein throughout AOB glomeruli, while Gαo expression is restricted to main olfactory glomeruli only. Our results suggest that the degeneration of the Gαo-expressing vomeronasal pathway has occurred independently at least four times in Eutheria, possibly related to the emergence of sexual dimorphisms and the ability of detecting the gender of conspecifics at distance.

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Phylogenetic tree of Eutheria showing approximate divergence times based on refs. [44], [45], [46].At least four independent events of deterioration of the Gαo -pathway in mammals may have occurred in the lineages leading to hyraxes, squirrels, Primates and Laurasiatheres (orange lines). Note that the species that lost the complete VNS (blank silhouettes and dashed lines) are nested in lineages that first lost the Gαo-pathway. Green silhouettes represent species with both Gαi2 and Gαo vomeronasal pathways.
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pone-0026436-g004: Phylogenetic tree of Eutheria showing approximate divergence times based on refs. [44], [45], [46].At least four independent events of deterioration of the Gαo -pathway in mammals may have occurred in the lineages leading to hyraxes, squirrels, Primates and Laurasiatheres (orange lines). Note that the species that lost the complete VNS (blank silhouettes and dashed lines) are nested in lineages that first lost the Gαo-pathway. Green silhouettes represent species with both Gαi2 and Gαo vomeronasal pathways.

Mentions: We have shown here that the Gαo-expressing pathway is absent in the AOB of species from two dimorphic lineages outside Primates and Laurasiatheria. Thus, considering current phylogenetic hypotheses [44], [45], [46], it can be safe to conclude that the loss of the Gαo-expressing vomeronasal pathway has occurred at least four times independently in mammals (Fig. 4). Whether these events of loss are related to the evolution of a gender recognition system based on non-vomeronasal cues (such as visual or auditory) is a possibility that deserves consideration.


Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals.

Suárez R, Fernández-Aburto P, Manger PR, Mpodozis J - PLoS ONE (2011)

Phylogenetic tree of Eutheria showing approximate divergence times based on refs. [44], [45], [46].At least four independent events of deterioration of the Gαo -pathway in mammals may have occurred in the lineages leading to hyraxes, squirrels, Primates and Laurasiatheres (orange lines). Note that the species that lost the complete VNS (blank silhouettes and dashed lines) are nested in lineages that first lost the Gαo-pathway. Green silhouettes represent species with both Gαi2 and Gαo vomeronasal pathways.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198400&req=5

pone-0026436-g004: Phylogenetic tree of Eutheria showing approximate divergence times based on refs. [44], [45], [46].At least four independent events of deterioration of the Gαo -pathway in mammals may have occurred in the lineages leading to hyraxes, squirrels, Primates and Laurasiatheres (orange lines). Note that the species that lost the complete VNS (blank silhouettes and dashed lines) are nested in lineages that first lost the Gαo-pathway. Green silhouettes represent species with both Gαi2 and Gαo vomeronasal pathways.
Mentions: We have shown here that the Gαo-expressing pathway is absent in the AOB of species from two dimorphic lineages outside Primates and Laurasiatheria. Thus, considering current phylogenetic hypotheses [44], [45], [46], it can be safe to conclude that the loss of the Gαo-expressing vomeronasal pathway has occurred at least four times independently in mammals (Fig. 4). Whether these events of loss are related to the evolution of a gender recognition system based on non-vomeronasal cues (such as visual or auditory) is a possibility that deserves consideration.

Bottom Line: We noted that the species that lost the Gαo pathway belong to Laurasiatheria and Primates lineages, both clades with ubiquitous sexual dimorphisms across species.We found that both species show uniform expression of Gαi2-protein throughout AOB glomeruli, while Gαo expression is restricted to main olfactory glomeruli only.Our results suggest that the degeneration of the Gαo-expressing vomeronasal pathway has occurred independently at least four times in Eutheria, possibly related to the emergence of sexual dimorphisms and the ability of detecting the gender of conspecifics at distance.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio de Neurobiología y Biología del Conocer, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Santiago, Chile. rsuarezsaa@gmail.com

ABSTRACT
In mammals, social and sexual behaviours are largely mediated by the vomeronasal system (VNS). The accessory olfactory bulb (AOB) is the first synaptic locus of the VNS and ranges from very large in Caviomorph rodents, small in carnivores and ungulates, to its complete absence in apes, elephants, most bats and aquatic species. Two pathways have been described in the VNS of mammals. In mice, vomeronasal neurons expressing Gαi2 protein project to the rostral portion of the AOB and respond mostly to small volatile molecules, whereas neurons expressing Gαo project to the caudal AOB and respond mostly to large non-volatile molecules. However, the Gαo-expressing pathway is absent in several species (horses, dogs, musk shrews, goats and marmosets) but no hypotheses have been proposed to date to explain the loss of that pathway. We noted that the species that lost the Gαo pathway belong to Laurasiatheria and Primates lineages, both clades with ubiquitous sexual dimorphisms across species. To assess whether similar events of Gαo pathway loss could have occurred convergently in dimorphic species we studied G-protein expression in the AOB of two species that independently evolved sexually dimorphic traits: the California ground squirrel Spermophilus beecheyi (Rodentia; Sciurognathi) and the cape hyrax Procavia capensis (Afrotheria; Hyracoidea). We found that both species show uniform expression of Gαi2-protein throughout AOB glomeruli, while Gαo expression is restricted to main olfactory glomeruli only. Our results suggest that the degeneration of the Gαo-expressing vomeronasal pathway has occurred independently at least four times in Eutheria, possibly related to the emergence of sexual dimorphisms and the ability of detecting the gender of conspecifics at distance.

Show MeSH
Related in: MedlinePlus