Distinct evolutionary trajectories of V1R clades across mouse species

Caitlin H Miller,Michael J Sheehan,Polly Campbell

doi:10.1186/s12862-020-01662-z

Caitlin H Miller, Michael J Sheehan + Show 1 more

Open Access

https://doi.org/10.1186/s12862-020-01662-z

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Abstract

BackgroundMany 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.ResultsWe 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.ConclusionAnalysis 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.

Highlights

Many animals rely heavily on olfaction to navigate their environment
Guided by the evolutionary patterns observed across clades, we identify and categorize receptors as interesting candidates for further functional work based on striking patterns of conservation or divergence (Additional File 3: Table S2)
In generating near-complete vomeronasal type-1 receptor (V1R) repertoires for 5 Mus species, we find evidence for previously described patterns of high gene turnover observed among divergent species

Summary

Introduction

Many animals rely heavily on olfaction to navigate their environment. Among rodents, olfaction is crucial for a wide range of social behaviors. Miller et al BMC Evolutionary Biology (2020) 20:99 among divergent species [19], VR evolution is characterized by rapid gene turnover wherein receptors are quickly gained and lost over evolutionary time [20,21,22]. This pattern of gene birth-and-death results in lineage-specific receptor repertoires [19]. Among three mammalian species (dog, opossum, and house mouse) there are virtually no one-to-one VR orthologs [19] This is perhaps not surprising given the broad evolutionary timescale examined. Some studies find evidence for positive selection and lineage-specific pseudogenization [30, 31], while another detects evidence of genetic drift and negative selection [32]

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