Comparative Genomic Analysis of the Pheromone Receptor Class 1 Family (V1R) Reveals Extreme Complexity in Mouse Lemurs (Genus, Microcebus) and a Chromosomal Hotspot across Mammals

Kelsie E. Hunnicutt, George P. Tiley, Rachel C. Williams, Peter A. Larsen, Marina B. Blanco, Rodin M. Rasoloarison, C. Ryan Campbell, Kevin Zhu, David W. Weisrock, Hiroaki Matsunami, Anne D. Yoder

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Sensory gene families are of special interest for both what they can tell us about molecular evolution and what they imply as mediators of social communication. The vomeronasal type-1 receptors (V1Rs) have often been hypothesized as playing a fundamental role in driving or maintaining species boundaries given their likely function as mediators of intraspecific mate choice, particularly in nocturnal mammals. Here, we employ a comparative genomic approach for revealing patterns of V1R evolution within primates, with a special focus on the small-bodied nocturnal mouse and dwarf lemurs of Madagascar (genera Microcebus and Cheirogaleus, respectively). By doubling the existing genomic resources for strepsirrhine primates (i.e.The lemurs and lorises), we find that the highly speciose and morphologically cryptic mouse lemurs have experienced an elaborate proliferation of V1Rs that we argue is functionally related to their capacity for rapid lineage diversification. Contrary to a previous study that found equivalent degrees of V1R diversity in diurnal and nocturnal lemurs, our study finds a strong correlation between nocturnality and V1R elaboration, with nocturnal lemurs showing elaborate V1R repertoires and diurnal lemurs showing less diverse repertoires. Recognized subfamilies among V1Rs show unique signatures of diversifying positive selection, as might be expected if they have each evolved to respond to specific stimuli. Furthermore, a detailed syntenic comparison of mouse lemurs with mouse (genus Mus) and other mammalian outgroups shows that orthologous mammalian subfamilies, predicted to be of ancient origin, tend to cluster in a densely populated region across syntenic chromosomes that we refer to as a V1R "hotspot."

Original languageEnglish (US)
Pages (from-to)3562-3579
Number of pages18
JournalGenome biology and evolution
Volume12
Issue number1
DOIs
StatePublished - Dec 16 2019

Bibliographical note

Funding Information:
We thank the Malagasy authorities for permission to conduct this research and Duke Lemur Center staff, especially Erin Ehmke, Bobby Schopler, and Cathy Williams, for providing the Microcebus murinus and Mirza zaza tissue samples. We are grateful to our colleagues at Baylor College of Medicine, Jeff Rogers and Kim Worley, for many insightful discussions of mouse lemur genomics. Phillip Brand, Jeff Thorne, and two anonymous reviewers provided critical reviews of the manuscript leading to its significant improvement. We thank Simon Gregory’s lab for preparing the 10⨯ Genomics libraries. We are grateful for the support of Duke Research Computing and the Duke Data Commons (NIH 1S10OD018164-01) and appreciate the donation of complimentary sequencing for Microcebus ravelobensis provided by the Duke GCB Sequencing Core. A.D.Y. gratefully acknowledges support from the John Simon Guggenheim Foundation and the Alexander von Humboldt Foundation during the writing phase of this project. The study was funded by the DTRI pilot program, NIH (R01 DC014423 to H.M.), NIH NRSA (5F31DC017394 to K.Z.), NSF (DEB-1354610 to A.D.Y. and D.W.W.), and Duke University startup funds (to A.D.Y.). This is Duke Lemur Center publication no. 1441.

Publisher Copyright:
© 2020 The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Keywords

  • Lemuriformes
  • V1R
  • gene family evolution
  • pheromone
  • synteny
  • vomeronasal system

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