Abstract
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.
Highlights
In placental mammals—the eutherian crown group consisting of the clades Afrotheria, Xenarthra, and Boreoeutheria [1]—optimal testicular function requires a temperature that is lower than the body temperature
By analyzing the evolution of two key genes that are required for gubernaculum development and function in 71 placental mammals, we found that both genes have loss-of-function mutations only in several testicond afrotherian species
The absence of shared inactivating mutations and our age estimates for the loss of relaxin/insulin-like family peptide receptor 2 (RXFP2) further suggest that testicondy evolved independently in afrotherian lineages at different time points. These results provide a molecular mechanism that explains the loss of testicular descent in afrotherian lineages and shows that testicular descent is the ancestral state for placental mammals and Afrotheria
Summary
In placental mammals—the eutherian crown group consisting of the clades Afrotheria, Xenarthra, and Boreoeutheria [1]—optimal testicular function requires a temperature that is lower than the body temperature. Testes are located in the lower abdomen in dolphins, true seals, pangolins, and other mammals. In these species, testicular cooling is achieved by vascular countercurrent heat exchanger systems, as observed in dolphin [4]; direct cooling with blood from the hind limbs, as observed in seals [5]; or testicular cooling may not be necessary, as these species have lower body temperatures [2, 6, 7]. The position of the testes in the lower abdomen or in the scrotum is the result of a developmental descent process (S1 Fig). Failure in any of the descent phases results in a pathological condition called cryptorchidism (absence of testes from the scrotum), which is a congenital birth defect observed at an appreciable frequency in human males (2%–4% at birth [11]) and other animals (up to 10% in male dogs [12], 2% in male cats [13], 2%–8% in male horses [14])
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
