Loss of RXFP2 and INSL3 genes in Afrotheria shows that testicular descent is the ancestral condition in placental mammals

  • Descent of testes from a position near the kidneys into the lower abdomen or into the scrotum is an important developmental process that occurs in all placental mammals, with the exception of five afrotherian lineages. Since soft-tissue structures like testes are not preserved in the fossil record and since key parts of the placental mammal phylogeny remain controversial, it has been debated whether testicular descent is the ancestral or derived condition in placental mammals. To resolve this debate, we used genomic data of 71 mammalian species and analyzed the evolution of two key genes (relaxin/insulin-like family peptide receptor 2 [RXFP2] and insulin-like 3 [INSL3]) that induce the development of the gubernaculum, the ligament that is crucial for testicular descent. We show that both RXFP2 and INSL3 are lost or nonfunctional exclusively in four afrotherians (tenrec, cape elephant shrew, cape golden mole, and manatee) that completely lack testicular descent. The presence of remnants of once functional orthologs of both genes in these afrotherian species shows that these gene losses happened after the split from the placental mammal ancestor. These “molecular vestiges” provide strong evidence that testicular descent is the ancestral condition, irrespective of persisting phylogenetic discrepancies. Furthermore, the absence of shared gene-inactivating mutations and our estimates that the loss of RXFP2 happened at different time points strongly suggest that testicular descent was lost independently in Afrotheria. Our results provide a molecular mechanism that explains the loss of testicular descent in afrotherians and, more generally, highlight how molecular vestiges can provide insights into the evolution of soft-tissue characters.
Metadaten
Author:Virag Sharma, Thomas Lehmann, Heiko Stuckas, Liane Funke, Michael Hiller
URN:urn:nbn:de:hebis:30:3-468277
DOI:https://doi.org/10.1371/journal.pbio.2005293
ISSN:1545-7885
ISSN:1544-9173
Pubmed Id:https://pubmed.ncbi.nlm.nih.gov/29953435
Parent Title (English):PLoS biology
Publisher:PLoS
Place of publication:Lawrence, KS
Contributor(s):Laurence Hurst
Document Type:Article
Language:English
Year of Completion:2018
Date of first Publication:2018/06/28
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2018/07/03
Tag:Afrotheria; Animal phylogenetics; Elephants; Eutheria; Hyraxes; Mammalian genomics; Mammals; Sequence alignment
Volume:16
Issue:(6): e2005293
Page Number:22
First Page:1
Last Page:22
Note:
Copyright: © 2018 Sharma et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
HeBIS-PPN:435980475
Institutes:Angeschlossene und kooperierende Institutionen / Senckenbergische Naturforschende Gesellschaft
Biowissenschaften / Institut für Ökologie, Evolution und Diversität
Dewey Decimal Classification:5 Naturwissenschaften und Mathematik / 59 Tiere (Zoologie) / 590 Tiere (Zoologie)
Sammlungen:Universitätspublikationen
Licence (German):License LogoCreative Commons - Namensnennung 4.0