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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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The accessory olfactory bulb (AOB) of the cape hyrax expresses Gαi2 but not Gαo.Similar to S. beecheyi, the AOB of Procavia capensis is located dorsocaudal to the main olfactory bulb (MOB) as shown in sagittal sections. Throughout its dorsocaudal extent, the AOB express Gαi2 (A, B) but not Gαo (D, E). MOB glomeruli express Gαo (F), but not Gαi2 (C). Interestingly, cell layering at the AOB (G, H) is not as clear as in rodents or as in its MOB (I). The dashed area in E shows the vomeronasal afferences; although Gαo is expressed to some extent at the glomerular layer (Gl) of the AOB, the vomeronasal nerve (VN) shows no Gαo expression. EP, external plexiform layer; Gr, granule cell layer; LOT, lateral olfactory tract; M/T, mitral/tufted cell layer. Dorsal is to the top and anterior is to the right. Scale bar: 500 µm in A, D and C; 200 µm in B, E and F; 100 µm in C, F and I.
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pone-0026436-g003: The accessory olfactory bulb (AOB) of the cape hyrax expresses Gαi2 but not Gαo.Similar to S. beecheyi, the AOB of Procavia capensis is located dorsocaudal to the main olfactory bulb (MOB) as shown in sagittal sections. Throughout its dorsocaudal extent, the AOB express Gαi2 (A, B) but not Gαo (D, E). MOB glomeruli express Gαo (F), but not Gαi2 (C). Interestingly, cell layering at the AOB (G, H) is not as clear as in rodents or as in its MOB (I). The dashed area in E shows the vomeronasal afferences; although Gαo is expressed to some extent at the glomerular layer (Gl) of the AOB, the vomeronasal nerve (VN) shows no Gαo expression. EP, external plexiform layer; Gr, granule cell layer; LOT, lateral olfactory tract; M/T, mitral/tufted cell layer. Dorsal is to the top and anterior is to the right. Scale bar: 500 µm in A, D and C; 200 µm in B, E and F; 100 µm in C, F and I.

Mentions: The AOB of P. capensis also occupies a somewhat small volume relative to its prominent MOB (Figure 3A, 3D and 3G). However, unlike other Afrotheres studied, such as tenrecs [14] and elephants [8], the MOB of P. capensis lacks an olfactory ventricle (Figure 3G). Gαi2 expression was confined to the VN and Gl layers of the AOB, throughout their entire extent (Figure 3A and 3B). There was no Gαi2 expression in axons arriving to MOB glomeruli via the ON (Figure 3C). As in S. beecheyi, Primates and Laurasiatheres, Gαo protein was absent from the VN layer and showed low expression in the parenchymal portion of the AOB (Figure 3D and 3E). However, MOB glomeruli and the ON showed Gαo expression (Figure 3F). Note that MOB layers are clearly stratified (Figure 3I), as seems to be the general condition of the mammalian MOB.


Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals.

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

The accessory olfactory bulb (AOB) of the cape hyrax expresses Gαi2 but not Gαo.Similar to S. beecheyi, the AOB of Procavia capensis is located dorsocaudal to the main olfactory bulb (MOB) as shown in sagittal sections. Throughout its dorsocaudal extent, the AOB express Gαi2 (A, B) but not Gαo (D, E). MOB glomeruli express Gαo (F), but not Gαi2 (C). Interestingly, cell layering at the AOB (G, H) is not as clear as in rodents or as in its MOB (I). The dashed area in E shows the vomeronasal afferences; although Gαo is expressed to some extent at the glomerular layer (Gl) of the AOB, the vomeronasal nerve (VN) shows no Gαo expression. EP, external plexiform layer; Gr, granule cell layer; LOT, lateral olfactory tract; M/T, mitral/tufted cell layer. Dorsal is to the top and anterior is to the right. Scale bar: 500 µm in A, D and C; 200 µm in B, E and F; 100 µm in C, F and I.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0026436-g003: The accessory olfactory bulb (AOB) of the cape hyrax expresses Gαi2 but not Gαo.Similar to S. beecheyi, the AOB of Procavia capensis is located dorsocaudal to the main olfactory bulb (MOB) as shown in sagittal sections. Throughout its dorsocaudal extent, the AOB express Gαi2 (A, B) but not Gαo (D, E). MOB glomeruli express Gαo (F), but not Gαi2 (C). Interestingly, cell layering at the AOB (G, H) is not as clear as in rodents or as in its MOB (I). The dashed area in E shows the vomeronasal afferences; although Gαo is expressed to some extent at the glomerular layer (Gl) of the AOB, the vomeronasal nerve (VN) shows no Gαo expression. EP, external plexiform layer; Gr, granule cell layer; LOT, lateral olfactory tract; M/T, mitral/tufted cell layer. Dorsal is to the top and anterior is to the right. Scale bar: 500 µm in A, D and C; 200 µm in B, E and F; 100 µm in C, F and I.
Mentions: The AOB of P. capensis also occupies a somewhat small volume relative to its prominent MOB (Figure 3A, 3D and 3G). However, unlike other Afrotheres studied, such as tenrecs [14] and elephants [8], the MOB of P. capensis lacks an olfactory ventricle (Figure 3G). Gαi2 expression was confined to the VN and Gl layers of the AOB, throughout their entire extent (Figure 3A and 3B). There was no Gαi2 expression in axons arriving to MOB glomeruli via the ON (Figure 3C). As in S. beecheyi, Primates and Laurasiatheres, Gαo protein was absent from the VN layer and showed low expression in the parenchymal portion of the AOB (Figure 3D and 3E). However, MOB glomeruli and the ON showed Gαo expression (Figure 3F). Note that MOB layers are clearly stratified (Figure 3I), as seems to be the general condition of the mammalian MOB.

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