The Microevolution of V1r Vomeronasal Receptor Genes in Mice

Park, Seong Hwan; Podlaha, Ondřej; Grus, Wendy E.; Zhang, Jianzhi

doi:10.1093/gbe/evr039

Cited by 33 publications

(30 citation statements)

References 65 publications

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“…Nevertheless, across all V1R clades only 10 gene losses are detected in the house mouse. This stands in contrast to a previous study examining the microevolution of V1Rs among Mus musculus subspecies, which detected a high frequency of null alleles (Park et al, 2011). We also identify a novel clade, which appears to have undergone pseudogenization in house mice and in rats.…”

Section: Discussioncontrasting

confidence: 99%

“…Prior research has generated controversy over what evolutionary forces mediate V1R evolution. Some studies detect evidence of positive selection and lineage-specific pseudogenization, while another study finds evidence for genetic drift and negative selection (Emes et al, 2004; Kurzweil et al, 2009; Park et al, 2011). Our data suggest that these seemingly contradictory results are not mutually exclusive.…”

Section: Discussionmentioning

confidence: 99%

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Distinct evolutionary trajectories of V1R clades across mouse species

Miller

Sheehan

Campbell

2019

Preprint

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29Background: Many animals rely heavily on olfaction to navigate their environment. Among rodents, 30 olfaction is crucial for a wide range of social behaviors. The vomeronasal olfactory system in particular 31 plays an important role in mediating social communication, including the detection of pheromones and 32 recognition signals. Currently, very few vomeronasal receptors have known ligands, which severely limits 33 our understanding of chemosensory-driven social communication. In this study we examine patterns of 34 vomeronasal type-1 receptor (V1R) evolution in the house mouse and related species within the genus 35 Mus. By exploring the evolution of these receptors, we provide insight into the functional roles of receptor 36 subtypes as well as the dynamics of gene family evolution. 37Results: We generated transcriptomes from the vomeronasal organs of 5 Mus species, and produced 38 high quality V1R repertoires for each species. We find that V1R clades in the house mouse and relatives 39 exhibit distinct evolutionary trajectories. Some clades are highly conserved, while others reveal patterns 40 of rapid evolutionary change. We identify putative species-specific gene expansions, including a dramatic 41 clade D expansion in the house mouse. While gene gains are abundant, we detect very few gene losses. 42We describe a novel V1R clade and highlight candidate receptors for future de-orphanization. Based on 43 clade-level evolutionary patterns, we identify receptor families that are strong candidates for detecting 44 social signals and predator cues. Our results further support the view that V1Rs are important for 45 detecting the physiological status of conspecifics, particularly female estrus cues. 46Conclusion: Analysis of clade-level evolution is critical for understanding species' chemosensory 47 adaptations. This study provides clear evidence that V1R clades are characterized by distinct 48 evolutionary trajectories. As receptor evolution is shaped by ligand identity, these results provide a

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Distinct evolutionary trajectories of V1R clades across mouse species

Miller

Sheehan

Campbell

2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Prior research has generated controversy over what evolutionary forces mediate V1R evolution. Some studies detect evidence of positive selection and lineage-speci c pseudogenization, while another study nds evidence for genetic drift and negative selection [30][31][32]. Our data suggest that these seemingly contradictory results are not mutually exclusive.…”

Section: V1r Clades Are Characterized By Distinct Evolutionary Trajecmentioning

confidence: 55%

Distinct evolutionary trajectories of V1R clades across mouse species

Miller

Campbell

Sheehan

2020

Preprint

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BACKGROUND: Many animals rely heavily on olfaction to navigate their environment. Among rodents, olfaction is crucial for a wide range of social behaviors. The vomeronasal olfactory system in particular plays an important role in mediating social communication, including the detection of pheromones and recognition signals. In this study we examine patterns of vomeronasal type-1 receptor (V1R) evolution in the house mouse and related species within the genus Mus . We report the extent of gene repertoire turnover and conservation among species and clades, as well as the prevalence of positive selection on gene sequences across the V1R tree. By exploring the evolution of these receptors, we provide insight into the functional roles of receptor subtypes as well as the dynamics of gene family evolution. RESULTS: We generated transcriptomes from the vomeronasal organs of 5 Mus species, and produced high quality V1R repertoires for each species. We find that V1R clades in the house mouse and relatives exhibit distinct evolutionary trajectories. We identify putative species-specific gene expansions, including a large clade D expansion in the house mouse. While gene gains are abundant, we detect very few gene losses. We describe a novel V1R clade and highlight candidate receptors for future study. We find evidence for distinct evolutionary processes across different clades, from largescale turnover to highly conserved repertoires. Patterns of positive selection are similarly variable, as some clades exhibit abundant positive selection while others display high gene sequence conservation. Based on clade-level evolutionary patterns, we identify receptor families that are strong candidates for detecting social signals and predator cues. Our results reveal clades with receptors detecting female reproductive status are among the most conserved across species, suggesting an important role in V1R chemosensation. CONCLUSION: Analysis of clade-level evolution is critical for understanding species’ chemosensory adaptations. This study provides clear evidence that V1R clades are characterized by distinct evolutionary trajectories. As receptor evolution is shaped by ligand identity, these results provide a framework for examining the functional roles of receptors.

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“…An analysis of 18 V1Rs between M. m. musculus and M. spretus revealed dynamic modulation in evolutionary pressures, including examples of positive selection and lineage-specific pseudogenisation [33]. Similarly, a recent study of 44 V1Rs in M. m. musculus and M. m. domesticus found evidence of genes shaped by negative selection and random drift, with a small proportion having evidence of positive selection [34]. Thus different rodent VR genes may be evolving under very different selective pressures, perhaps depending on the functional nature of their ligands; though whether these correlate within VR families, clades or even clusters is unknown.…”

Section: Introductionmentioning

confidence: 99%

Genomic variation in the vomeronasal receptor gene repertoires of inbred mice

et al. 2012

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BackgroundVomeronasal receptors (VRs), expressed in sensory neurons of the vomeronasal organ, are thought to bind pheromones and mediate innate behaviours. The mouse reference genome has over 360 functional VRs arranged in highly homologous clusters, but the vast majority are of unknown function. Differences in these receptors within and between closely related species of mice are likely to underpin a range of behavioural responses. To investigate these differences, we interrogated the VR gene repertoire from 17 inbred strains of mice using massively parallel sequencing.ResultsApproximately half of the 6222 VR genes that we investigated could be successfully resolved, and those that were unambiguously mapped resulted in an extremely accurate dataset. Collectively VRs have over twice the coding sequence variation of the genome average; but we identify striking non-random distribution of these variants within and between genes, clusters, clades and functional classes of VRs. We show that functional VR gene repertoires differ considerably between different Mus subspecies and species, suggesting these receptors may play a role in mediating behavioural adaptations. Finally, we provide evidence that widely-used, highly inbred laboratory-derived strains have a greatly reduced, but not entirely redundant capacity for differential pheromone-mediated behaviours.ConclusionsTogether our results suggest that the unusually variable VR repertoires of mice have a significant role in encoding differences in olfactory-mediated responses and behaviours. Our dataset has expanded over nine fold the known number of mouse VR alleles, and will enable mechanistic analyses into the genetics of innate behavioural differences in mice.

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The Microevolution of V1r Vomeronasal Receptor Genes in Mice

Cited by 33 publications

References 65 publications

Distinct evolutionary trajectories of V1R clades across mouse species

Distinct evolutionary trajectories of V1R clades across mouse species

Distinct evolutionary trajectories of V1R clades across mouse species

Genomic variation in the vomeronasal receptor gene repertoires of inbred mice

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