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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 Gao-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 Gao-pathway. Green silhouettes represent species with both Gai2 and Gao vomeronasal pathways. doi:10.1371/journal.pone.0026436.g004
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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 bee...
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Context 1
... shown here that the Gao-expressing pathway is absent in the AOB of species from two dimorphic lineages outside Primates and Laurasiatheria. Thus, considering current phyloge- netic hypotheses [44,45,46], it can be safe to conclude that the loss of the Gao-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 ...
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... believe it reflects additional ecological constraints related to capybaras semiaquatic habits and/or male-male chemosignalling, plus a reduced dependence on vision associated to dense vegetation and their cathemeral/crepuscular habits. Anyhow, it is interesting to note that all species that underwent a complete loss the VNS belong to lineages that first lost the Gao-expressing pathway (Figure 4). Interestingly, the differentiation of developing vomero- nasal neurons into one of each pathway is under control of the transcription factor Ctip2/Bcl11b, and mice lacking this protein show a deficit in the Gao-expressing pathway and an increase in the Gai2-positive neurons [55]. ...
Citations
... This significance is reinforced by both neurochemical (Shinohara et al., 1992) and genomic studies (Dulac & Axel, 1995;Herrada & Dulac, 1997;Matsunami & Buck, 1997;Ryba & Tirindelli, 1997) in rodents, which consistently associate the Gαi2 protein with the expression of the V1Rs receptor family in the VNS, whereas the Gαo protein is linked to the V2Rs family. Subsequent research has revealed the absence of the Gαo pathway in various mammals, including both Laurasiatheria and Primates (Suárez, Fernández-Aburto, et al., 2011;Takigami et al., 2000). Nevertheless, studies focusing on G protein expression in the VNS of Carnivora have been a point of debate. ...
Wolves, akin to their fellow canids, extensively employ chemical signals for various aspects of communication, including territory maintenance, reproductive synchronisation and social hierarchy signalling. Pheromone‐mediated chemical communication operates unconsciously among individuals, serving as an innate sensory modality that regulates both their physiology and behaviour. Despite its crucial role in the life of the wolf, there is a lacuna in comprehensive research on the neuroanatomical and physiological underpinnings of chemical communication within this species. This study investigates the vomeronasal system (VNS) of the Iberian wolf, simultaneously probing potential alterations brought about by dog domestication. Our findings demonstrate the presence of a fully functional VNS, vital for pheromone‐mediated communication, in the Iberian wolf. While macroscopic similarities between the VNS of the wolf and the domestic dog are discernible, notable microscopic differences emerge. These distinctions include the presence of neuronal clusters associated with the sensory epithelium of the vomeronasal organ (VNO) and a heightened degree of differentiation of the accessory olfactory bulb (AOB). Immunohistochemical analyses reveal the expression of the two primary families of vomeronasal receptors (V1R and V2R) within the VNO. However, only the V1R family is expressed in the AOB. These findings not only yield profound insights into the VNS of the wolf but also hint at how domestication might have altered neural configurations that underpin species‐specific behaviours. This understanding holds implications for the development of innovative strategies, such as the application of semiochemicals for wolf population management, aligning with contemporary conservation goals.
... ;https://doi.org/10.1101.09.14.557816 doi: bioRxiv preprint Dulac 1997Matsunami and Buck 1997;Ryba and Tirindelli 1997) in rodents, which have consistently indicated that the Gαi2 protein is tied to the expression of the V1Rs receptor family in the VNS, whereas the Gαo protein is linked to the V2Rs family. Subsequent research revealed the absence of the Gαo pathway in various mammals, including both Laurasiatheria and Primates (Takigami et al. 2000;Suárez et al. 2011a). However, the sparse studies focusing on G protein expression in the VNS of Carnivora have been a point of debate. ...
Wolves, like other canids, extensively use chemical signals for various aspects of communication, including territory maintenance, reproductive synchronization, and social hierarchy signaling. Pheromone-mediated chemical communication operates unconsciously among individuals, acting as a mysterious sixth sense that regulates both their physiology and behavior. Despite their crucial role in the life of the wolf, there is a surprising lack of comprehensive research on the neuroanatomical and physiological bases of chemical communication in wolves.
This study delves into the Iberian wolf vomeronasal system (VNS) and examines potential changes brought about by dog domestication. Our findings show that the Iberian wolf possesses a fully functional VNS vital for pheromone-mediated communication. While macroscopic similarities between the wolf and domestic dog VNS are observed, there are notable microscopic differences. These include the presence of neuronal clusters associated with the sensory epithelium of the vomeronasal organ (VNO) and a higher differentiation degree of the accessory olfactory bulb (AOB). Immunohistochemical markers reveal the expression of the two main families of vomeronasal receptors (V1R and V2R) in the VNO. However, only the V1R family is expressed in the AOB.
These findings not only provide deep insights into the VNS of the wolf but also hint at how domestication might have altered neural configurations that underpin species-specific behaviors. This understanding has implications for innovative strategies, such as employing semiochemicals for wolf population management, aligning with modern conservation goals.
... We used specific antibodies against the α subunits of the Gi2 and Go proteins to characterize the expression of the vomeronasal receptors, V1R and V2R, respectively (Dulac & Axel, 1995;Ryba & Tirindelli, 1997). An investigation of G protein expression and distribution in the goat VNS revealed, for the first time, that the Go pathway was absent in some species (Takigami, 2000), a finding that was subsequently confirmed in numerous mammals, including Laurasiatheria and Primates (Suárez et al., 2011). However, discrepancies between gene sequencing and immunohistochemical studies have been documented, particularly in the order Carnivora. ...
Dama gazelle is a threatened and rarely studied species found primarily in northern Africa. Human pressure has depleted the dama gazelle population from tens of thousands to a few hundred individuals. Since 1970, a founder population consisting of the last 17 surviving individuals in Western Sahara has been maintained in captivity, reproducing naturally. In preparation for the future implementation of assisted reproductive technology, certain aspects of dama gazelle reproductive biology have been established. However, the role played by semiochemical‐mediated communications in the sexual behavior of dama gazelle remains unknown due partially to a lack of a neuroanatomical or morphofunctional characterization of the dama gazelle vomeronasal organ (VNO), which is the sensory organ responsible for pheromone processing. The present study characterized the dama gazelle VNO, which appears fully equipped to perform neurosensory functions, contributing to current understanding of interspecies VNO variability among ruminants. By employing histological, lectin‐histochemical, and immunohistochemical techniques, we conducted a detailed morphofunctional evaluation of the dama gazelle VNO along its entire longitudinal axis. Our findings of significant structural and neurochemical transformation along the entire VNO suggest that future studies of the VNO should take a similar approach. The present study contributes to current understanding of dama gazelle VNO, providing a basis for future studies of semiochemical‐mediated communications and reproductive management in this species.
Research Highlights
This exhaustive immunohistological study of the vomeronasal organ (VNO) of the dama gazelle provides the first evidence of notable differences in the expression of neuronal markers along the rostrocaudal axis of the VNO.
This provides a morphological basis for the implementation of pheromones in captive populations of dama gazelle.
... /2023 To characterize the expression of the two major families of vomeronasal receptors, V1R and V2R, respectively (Dulac & Axel, 1995;Ryba & Tirindelli, 1997), specific antibodies against the α subunit of Gi2 and Go proteins are particularly useful. The investigation of G protein expression and distribution in the goat VNS (Takigami, 2000) revealed, for the first time, that the Go pathway had disappeared in some species, a finding that was subsequently confirmed in numerous mammals, including Laurasiatheria and Primates (Suárez et al., 2011). However, there have been observed discrepancies between gene sequencing and immunohistochemical studies, mainly in the Order Carnivora, where Dennis et al. (2003) in the dog and Ortiz-Leal et al. (2020) in the fox observed immunopositive labelling in the vomeronasal neurosensory epithelium using both anti-Gαi2 and anti-Gαo antibodies. ...
The dama gazelle is a threatened and scarcely studied species of northern Africa. Human pressure has depleted the population of dama gazelles from tens of thousands to a few hundred individuals. Since 1970, after deriving from a founder population of the last 17 surviving individuals in the Western Sahara, it has been reproduced naturally in captivity. Although certain aspects of the reproductive biology of the dama gazelle have been established in preparation for the future implementation of assisted reproductive technology there is a lack of information regarding the role of semiochemical-mediated communication in the sexual behavior of the dama gazelle. This is partially due to the lack of a neuroanatomical and morphofunctional characterization of the dama gazelle vomeronasal organ (VNO); the sensory organ responsible for the processing of pheromones. This study aims to determine the presence in the dama gazelle of a VNO fully equipped to carry out its neurosensory function and to contribute to the understanding of the interspecific variability of the VNO of ruminants. Employing histological, lectin-histochemical and immunohistochemical techniques we have performed a detailed morphofunctional evaluation of the dama gazelle VNO along its entire longitudinal axis. The findings suggest that studies of the VNO should take a similar approach, as there are significant structural and neurochemical transformations that the organ exhibits as a whole. This study contributes to the understanding of the VNO in dama gazelles and provides a basis for future studies on semiochemical-mediated communication and reproductive management of this species.
... However, the types of vomeronasal systems in animal species even in the same order should be carefully verified. In fact, although most rodents have a segregated vomeronasal system (Jia and Halpern, 1996;Shinohara et al., 1992), squirrels have a uniform system (Suárez et al., 2011). Therefore, further investigation using more species is needed to clarify the lineage of the mammalian vomeronasal system. ...
Artiodactyl livestock animals have a vomeronasal system that detects pheromones. Vomeronasal receptors comprise type 1 (V1R) coupled with G protein α-i2 (Gαi2) and type 2 (V2R) coupled with G protein α-o (Gαo). Laboratory rodents have two segregated V1R and V2R pathways that reach separately to the accessory olfactory bulb (AOB). In contrast, the AOBs of goats and sheep are entirely positive for Gαi2, indicating that they have only the V1R pathway. However, we detected a few V2R genes in the genome of cattle, goats, sheep and pigs by genome assembly. Thus, we immunohistochemically analyzed the AOBs of cattle and pigs to confirm which type of the vomeronasal system is present in artiodactyl livestock species. The glomerular layer of the AOB in cattle and pigs was entirely positive for anti-Gαi2 and weakly positive for anti-Gαo, as in the V1R uniform type of vomeronasal system in other mammal species. These findings indicated that artiodactyl livestock species have a uniform type of vomeronasal system composing the V1R pathway. Therefore, caution is advised when extrapolating knowledge of laboratory rodents with two vomeronasal pathways to livestock animals that have one.
... The segregated type, in which the VN neurons express both G proteins, Gαi2 and Gαo, is observed in Rodents, such as mouse, rat, octodon , guinea pig (Takigami et al. 2004), and capybara (Suarez et al. 2011b;Torres et al. 2020); Lagomorpha, such as rabbit (Villamayor et al. 2018); Marsupials, including opossum (Halpern et al. 1995); and tenrecs ). The uniform type, in which the VN neurons only express a single G protein subtype, specifically the Gαi2 subunit, can be observed in goat (Takigami et al. 2000), sheep (Salazar et al. 2007), dog (Salazar et al. 2013), horse, marmoset, musk shrew (Takigami et al. 2004), squirrel, hyrax (Suarez et al. 2011a), and hippopotamus (Kondoh et al. 2017b). ...
... The absence of the V2R pathway in the uniform model has been hypothesized to be closely related to the appearance of sexual dimorphism in mammals (Suarez et al. 2011a). This deterioration has become a challenge for understanding the role played by the VNS in mammals, and this complex panorama was further convoluted by the appearance of a study of the VNS in the marsupial tammar wallaby, Notamacropus eugenii (Schneider et al. 2012). ...
The study of the α-subunit of Gi2 and Go proteins in the accessory olfactory bulb (AOB) was crucial for the identification of the two main families of vomeronasal receptors, V1R and V2R. Both families are expressed in the rodent and lagomorph AOBs, according to a segregated model characterized by topographical anteroposterior zonation. Many mammal species have suffered from the deterioration of the Gαo pathway and are categorized as belonging to the uniform model. This scenario has been complicated by characterization of the AOB in the tammar wallaby, Notamacropus eugenii , which appears to follow a third model of vomeronasal organization featuring exclusive Gαo protein expression, referred to as the intermediate model, which has not yet been replicated in any other species. Our morphofunctional study of the vomeronasal system (VNS) in Bennett’s wallaby, Notamacropus rufogriseus, provides further information regarding this third model of vomeronasal transduction. A comprehensive histological, lectin, and immunohistochemical study of the Bennett’s wallaby VNS was performed. Anti-Gαo and anti-Gαi2 antibodies were particularly useful because they labeled the transduction cascade of V2R and V1R receptors, respectively. Both G proteins showed canonical immunohistochemical labeling in the vomeronasal organ and the AOB, consistent with the anterior–posterior zonation of the segregated model. The lectin Ulex europaeus agglutinin selectively labeled the anterior AOB, providing additional evidence for the segregation of vomeronasal information in the wallaby. Overall, the VNS of the Bennett’s wallaby shows a degree of differentiation and histochemical and neurochemical diversity comparable to species with greater VNS development. The existence of the third intermediate type in vomeronasal information processing reported in Notamacropus eugenii is not supported by our lectin-histochemical and immunohistochemical findings in Notamacropus rufogriseus .
... This segregated projection has been described in Rodentia [104][105][106], Marsupialia [82,107], and Afrosoricidae [108]. However, this is not a uniform feature among mammals, as the Gαo pathway has deteriorated in several orders, including Carnivora, such as in dogs [59], cats [90], and foxes [109]; Artiodactyla [110]; Perissodactyla; Insectivora; Primates [111]; Hyracoidea [112]; and some Rodentia species, such as squirrels [112]. ...
... This segregated projection has been described in Rodentia [104][105][106], Marsupialia [82,107], and Afrosoricidae [108]. However, this is not a uniform feature among mammals, as the Gαo pathway has deteriorated in several orders, including Carnivora, such as in dogs [59], cats [90], and foxes [109]; Artiodactyla [110]; Perissodactyla; Insectivora; Primates [111]; Hyracoidea [112]; and some Rodentia species, such as squirrels [112]. ...
We approached the study of the main (MOB) and accessory olfactory bulbs (AOB) of the meerkat (Suricata suricatta) aiming to fill important gaps in knowledge regarding the neuroanatomical basis of olfactory and pheromonal signal processing in this iconic species. Microdissection techniques were used to extract the olfactory bulbs. The samples were subjected to hematoxylin-eosin and Nissl stains, histochemical (Ulex europaeus agglutinin, Lycopersicon esculentum agglutinin) and immunohistochemical labelling (Gαo, Gαi2, calretinin, calbindin, olfactory marker protein, glial fibrillary acidic protein, microtubule-associated protein 2, SMI-32, growth-associated protein 43). Microscopically, the meerkat AOB lamination pattern is more defined than the dog’s, approaching that described in cats, with well-defined glomeruli and a wide mitral-plexiform layer, with scattered main cells and granular cells organized in clusters. The degree of lamination and development of the meerkat MOB suggests a macrosmatic mammalian species. Calcium-binding proteins allow for the discrimination of atypical glomerular subpopulations in the olfactory limbus between the MOB and AOB. Our observations support AOB functionality in the meerkat, indicating chemosensory specialization for the detection of pheromones, as identified by the characterization of the V1R vomeronasal receptor family and the apparent deterioration of the V2R receptor family.
... The segregated model, in which NVNs express both Gαi2 and Gαo, was identi ed in Rodentia, in species of mouse, rat, octodon ( (Halpern et al. 1995). The uniform model, in which the NVNs only express a single G protein subtype, Gαi2, was observed for goats (Takigami et al. 2000), sheep (Salazar et al. 2007), dogs (Salazar et al. 2013), horses, musk shrews (Takigami et al. 2004), squirrels (Suarez et al. 2011a), and marmosets (Moriya-Ito et al. 2018). ...
... The absence of the V2R pathway in the uniform model has been hypothesized to be closely related to the appearance of sexual dimorphism in mammals (Suarez et al. 2011a). This deterioration has become a challenge for understanding the role played by the VNS in mammals, and this complex panorama was further convoluted by the appearance of a study of the VNS in the marsupial tammar wallaby, Macropus eugenii (Schneider et al. 2012). ...
The study of the α-subunit of Gi2 and Go proteins in the accessory olfactory bulb (AOB) was crucial for the identification of the two main families of vomeronasal receptors, V1R and V2R. Both families are expressed in the rodent and lagomorph AOBs, according to a segregated model characterized by topographical anteroposterior zonation. Many mammal species have suffered from the deterioration of the Gαo pathway and are categorized as belonging to the uniform model. This scenario has been complicated by characterization of the AOB in the tammar wallaby, Macropus eugenii, which appears to follow a third model of vomeronasal organization featuring exclusive Gαo protein expression, referred to as the intermediate model, which has not yet been replicated in any other species. Our morphofunctional study of the vomeronasal system (VNS) in Bennett’s wallaby, Macropus rufogriseus, provides further information regarding this third model of vomeronasal transduction.
A comprehensive histological, lectin, and immunohistochemical study of the Bennett’s wallaby VNS was performed. Anti-Gαo and anti-Gαi2 antibodies were particularly useful because they labeled the transduction cascade of V2R and V1R receptors, respectively. Both G proteins showed canonical immunohistochemical labeling in the vomeronasal organ and the AOB, consistent with the anterior-posterior zonation of the segregated model. The lectin Ulex europaeus agglutinin selectively labeled the anterior AOB, providing additional evidence for the segregation of vomeronasal information in the wallaby.
Overall, the VNS of the Bennett’s wallaby shows a degree of differentiation and histochemical and neurochemical diversity comparable to species with greater VNS development, which does not support the existence of a third “intermediate” type of vomeronasal information processing.
... Some NWMs have a complex VNO, such as Owl monkeys (Aotus) (Smith et al., 2011), which have not been documented displaying SSSB. Other NWM, like marmosets (Callithrix), have lost function of some VNO-related genes, such as pheromone receptors (e.g., V2R genes) and g-protein second messengers (e.g., G α o) (Suárez, Fernández-Aburto, Manger, & Mpodozis, 2011;Young & Trask, 2007), which partially rely on TRPC2 to propagate action potentials (Stowers & Spehr, 2015), and they express limited SSSB (Rothe, 1975). However, presence of these other VNO-related genes among NWMs has not been extensively examined and G α o KO mice don't show SSSB ; thus its loss and SSSB expression in marmosets may be coincidental. ...
Primate same-sex sexual behavior (SSSB) is rarely observed in strepsirrhine species, and only somewhat more common in platyrrhines, but is observed in nearly all catarrhine species, including humans, suggesting the common catarrhine ancestor as the origin of routine SSSB. In mice, disruption of the transient receptor potential cation channel 2 (TRPC2) gene, which is crucial for transducing chemosensory signals from pheromones in the vomeronasal organ, greatly increased the likelihood of SSSB. We note that catarrhine primates share a common deleterious mutation in this gene, indicating that the protein was dysfunctional in the common catarrhine ancestral primate approximately 25 mya (million years ago). We hypothesize that the loss of this protein for processing pheromonal signals in males and females made SSSB more likely in a primate ancestral species by effectively lifting a pheromonally mediated barrier to SSSB and that this was an important precursor to the evolution of such behavior in humans. Additional comparisons between SSSB and the functional status of the TRPC2 gene or related proteins across primate species could lend support to or falsify this hypothesis. Our current research indicates that loss of TRPC2 function in developing mice leads to the loss or attenuation of sexually dimorphisms in the adult brain, which may help us to understand the biological underpinnings of SSSB. Our hypothesis offers an ultimate evolutionary explanation for SSSB in humans.
... In contrast, birds, bats (with the exception of the family of Phyllostomidae), cetaceans, old world monkeys, apes, and humans do not possess a functional or anatomically evident VNO (Eisthen 1992;Zhang and Webb 2003;Bhatnagar and Smith 2007;Zhao et al. 2011;Smith et al. 2014;Taniguchi 2014;Yohe et al. 2019). In the Laurasiatheria superorder, which includes Carnivora (cat and dog), Artiodactyla (sheep, pig, and cow), Perissodactyla (horse and goat), and Strepsirrhini primates (lemurs), a transitional situation can be observed, with a less complex VNO, in terms of receptors and transduction molecules (Salazar et al. 1996(Salazar et al. , 2013Takigami et al. 2000;Suarez et al. 2011;Taniguchi 2014;Silva and Antunes 2017;Ibrahim 2018). The anatomical and molecular organization of the vomeronasal system. ...
Communication between individuals is critical for species survival, reproduction, and expansion. Most terrestrial species, with the exception of humans who predominantly use vision and phonation to create their social network, rely on the detection and decoding of olfactory signals, which are widely known as pheromones. These chemosensory cues originate from bodily fluids, causing attractive or avoidance behaviors in subjects of the same species. Intraspecific pheromone signaling is then crucial to identify sex, social ranking, individuality, and health status, thus establishing hierarchies and finalizing the most efficient reproductive strategies. Indeed, all these features require fine tuning of the olfactory systems to detect molecules containing this information. To cope with this complexity of signals, tetrapods have developed dedicated olfactory subsystems that refer to distinct peripheral sensory detectors, called the main olfactory and the vomeronasal organ, and two minor structures, namely the septal organ of Masera and the Grueneberg ganglion. Among these, the vomeronasal organ plays the most remarkable role in pheromone coding by mediating several behavioral outcomes that are critical for species conservation and amplification. In rodents, this organ is organized into two segregated neuronal subsets that express different receptor families. To some extent, this dichotomic organization is preserved in higher projection areas of the central nervous system, suggesting, at first glance, distinct functions for these two neuronal pathways. Here, I will specifically focus on this issue and discuss the role of vomeronasal receptors in mediating important innate behavioral effects through the recognition of pheromones and other biological chemosignals.
