Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved November 26, 2018 (received for review August 14, 2018)
Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has evolved numerous times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuroendocrine pathways play conserved roles in regulating social affiliation and parental care, but little is known about the evolution of the neuromolecular mechanisms underlying monogamy. Here, we show that shared transcriptomic profiles are associated with monogamy across vertebrates and discuss the importance of our discovery for understanding the origins of behavioral diversity. We compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of mice, voles, parid songbirds, frogs, and cichlid fishes. Our results provide evidence of a universal transcriptomic code underlying monogamy in vertebrates.
Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.
Author contributions: R.L.Y., L.A.O., and H.A.H. designed research; R.L.Y., M.H.F., N.F.O.-P., V.N.O., S.M.P., Á.P., C.L.R.-Z., K.S., T.S., B.C.T., A.O.U., G.Z., L.A.O., and H.A.H. performed research; R.L.Y., L.A.O., and H.A.H. analyzed data; and R.L.Y. and H.A.H. wrote the paper.
The authors declare no conflict of interest
This article is a PNAS Direct Submission.
Data deposition: All sequence data in this publication have been deposited in National Center for Biotechnology Information Gene Expression Omnibus, https://www.ncbi.nlm.nih.gov/geo (SuperSeries GSE123301, accession nos. GSM3499527–GSM3499536). All metadata and protocols/scripts are available on the Texas Data Repository (https://dataverse.tdl.org/dataverse/monogamy).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1813775116/-/DCSupplemental.
Published under the PNAS license.
