Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals
Abstract Background The mammalian testis is an important male exocrine gland and spermatozoa-producing organ that usually lies in extra-abdominal scrotums to provide a cooler environment for spermatogenesis and sperm storage. Testicles sometimes fail to descend, leading to cryptorchidism. However, c...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2021-02-01
|
Series: | BMC Ecology and Evolution |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12862-021-01753-5 |
id |
doaj-27ccdd3c34ee481e8790894eee2c35eb |
---|---|
record_format |
Article |
spelling |
doaj-27ccdd3c34ee481e8790894eee2c35eb2021-08-29T11:06:11ZengBMCBMC Ecology and Evolution2730-71822021-02-0121111410.1186/s12862-021-01753-5Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammalsSimin Chai0Ran Tian1Juanjuan Bi2Shixia Xu3Guang Yang4Wenhua Ren5School of Life Sciences, Nanjing Normal UniversitySchool of Life Sciences, Nanjing Normal UniversitySchool of Life Sciences, Nanjing Normal UniversitySchool of Life Sciences, Nanjing Normal UniversitySchool of Life Sciences, Nanjing Normal UniversitySchool of Life Sciences, Nanjing Normal UniversityAbstract Background The mammalian testis is an important male exocrine gland and spermatozoa-producing organ that usually lies in extra-abdominal scrotums to provide a cooler environment for spermatogenesis and sperm storage. Testicles sometimes fail to descend, leading to cryptorchidism. However, certain groups of mammals possess inherently ascrotal testes (i.e. testes that do not descend completely or at all) that have the same physiological functions as completely descended scrotal testes. Although several anatomical and hormonal factors involved in testicular descent have been studied, there is still a paucity of comprehensive research on the genetic mechanisms underlying the evolution of testicular descent in mammals and how mammals with ascrotal testes maintain their reproductive health. Results We performed integrative phenotypic and comparative genomic analyses of 380 cryptorchidism-related genes and found that the mammalian ascrotal testes trait is derived from an ancestral scrotal state. Rapidly evolving genes in ascrotal mammals were enriched in the Hedgehog pathway—which regulates Leydig cell differentiation and testosterone secretion—and muscle development. Moreover, some cryptorchidism-related genes in ascrotal mammals had undergone positive selection and contained specific mutations and indels. Genes harboring convergent/parallel amino acid substitutions between ascrotal mammals were enriched in GTPase functions. Conclusions Our results suggest that the scrotal testis is an ancestral state in mammals, and the ascrotal phenotype was derived multiple times in independent lineages. In addition, the adaptive evolution of genes involved in testicular descent and the development of the gubernaculum contributed to the evolution of ascrotal testes. Accurate DNA replication, the proper segregation of genetic material, and appropriate autophagy are the potential mechanisms for maintaining physiological normality during spermatogenesis in ascrotal mammals. Furthermore, the molecular convergence of GTPases is probably a mechanism in the ascrotal testes of different mammals. This study provides novel insights into the evolution of the testis and scrotum in mammals and contributes to a better understanding of the pathogenesis of cryptorchidism in humans.https://doi.org/10.1186/s12862-021-01753-5Testicular descentCryptorchidism-related genesMolecular convergenceRapid evolution |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Simin Chai Ran Tian Juanjuan Bi Shixia Xu Guang Yang Wenhua Ren |
spellingShingle |
Simin Chai Ran Tian Juanjuan Bi Shixia Xu Guang Yang Wenhua Ren Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals BMC Ecology and Evolution Testicular descent Cryptorchidism-related genes Molecular convergence Rapid evolution |
author_facet |
Simin Chai Ran Tian Juanjuan Bi Shixia Xu Guang Yang Wenhua Ren |
author_sort |
Simin Chai |
title |
Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
title_short |
Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
title_full |
Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
title_fullStr |
Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
title_full_unstemmed |
Rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
title_sort |
rapid evolution and molecular convergence in cryptorchidism-related genes associated with inherently undescended testes in mammals |
publisher |
BMC |
series |
BMC Ecology and Evolution |
issn |
2730-7182 |
publishDate |
2021-02-01 |
description |
Abstract Background The mammalian testis is an important male exocrine gland and spermatozoa-producing organ that usually lies in extra-abdominal scrotums to provide a cooler environment for spermatogenesis and sperm storage. Testicles sometimes fail to descend, leading to cryptorchidism. However, certain groups of mammals possess inherently ascrotal testes (i.e. testes that do not descend completely or at all) that have the same physiological functions as completely descended scrotal testes. Although several anatomical and hormonal factors involved in testicular descent have been studied, there is still a paucity of comprehensive research on the genetic mechanisms underlying the evolution of testicular descent in mammals and how mammals with ascrotal testes maintain their reproductive health. Results We performed integrative phenotypic and comparative genomic analyses of 380 cryptorchidism-related genes and found that the mammalian ascrotal testes trait is derived from an ancestral scrotal state. Rapidly evolving genes in ascrotal mammals were enriched in the Hedgehog pathway—which regulates Leydig cell differentiation and testosterone secretion—and muscle development. Moreover, some cryptorchidism-related genes in ascrotal mammals had undergone positive selection and contained specific mutations and indels. Genes harboring convergent/parallel amino acid substitutions between ascrotal mammals were enriched in GTPase functions. Conclusions Our results suggest that the scrotal testis is an ancestral state in mammals, and the ascrotal phenotype was derived multiple times in independent lineages. In addition, the adaptive evolution of genes involved in testicular descent and the development of the gubernaculum contributed to the evolution of ascrotal testes. Accurate DNA replication, the proper segregation of genetic material, and appropriate autophagy are the potential mechanisms for maintaining physiological normality during spermatogenesis in ascrotal mammals. Furthermore, the molecular convergence of GTPases is probably a mechanism in the ascrotal testes of different mammals. This study provides novel insights into the evolution of the testis and scrotum in mammals and contributes to a better understanding of the pathogenesis of cryptorchidism in humans. |
topic |
Testicular descent Cryptorchidism-related genes Molecular convergence Rapid evolution |
url |
https://doi.org/10.1186/s12862-021-01753-5 |
work_keys_str_mv |
AT siminchai rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals AT rantian rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals AT juanjuanbi rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals AT shixiaxu rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals AT guangyang rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals AT wenhuaren rapidevolutionandmolecularconvergenceincryptorchidismrelatedgenesassociatedwithinherentlyundescendedtestesinmammals |
_version_ |
1721187126354116608 |