Abstract
During embryonic development in mammals, the testicles generally descend into the scrotum, making the testicular temperature 2–4 °C lower than the core temperature via heat exchange and clearance, and thus more beneficial for normal spermatogenesis. Failure to descend, known as cryptorchidism, carries a series of risks such as infertility and testicular cancer. However, some mammals have evolved abdominal testes while maintaining healthy reproduction. To explore the underlying molecular mechanism, we conducted comparative genomic analyses and functional assays on the spermatogenesis-related ubiquitin–proteasome system (UPS) genes essential to sperm formation in representative laurasiatherians. Here, positive selection and rapid evolution of spermatogenesis-related UPS genes were identified in the abdominal testicular laurasiatherians. Moreover, potential convergent amino acids were found between distantly related species with similar abdominal testicles and functional analyses showed RNF8 (V437I) in abdominal testicular species (437I) has a stronger ubiquitination ability, which suggests that the mammals with abdominal testes might exhibit enhanced sperm cell histone clearance to maintain sperm formation. This evidence implies that, in response to “cryptorchidism injury”, spermatogenesis-related UPS genes in the abdominal testicular species might have undergone adaptive evolution to stabilize sperm formation. Thus, our study could provide some novel insights into the reproductive adaptation in abdominal testicular mammals.
Highlights
The testis, the organ in which spermatogenesis begins, is important for male reproduction
UBA1/UBE1, an E1, initiates the cascade of ubiquitin–proteasome system (UPS) and is involved in male reproduction via spermatogenesis [20]; UBE2A/HR6A, an E2, is required for the maintenance of X chromosome silencing in spermatocytes and spermatids [21]; RNF8, an E3, participates in sperm cell nucleosome remodeling through the ubiquitination of histones [22,23]; PSMA8, a testis-specific 20S core proteasome subunit, degrades pro-meiotic I protein during spermatogenesis [24]; UCHL3, a deubiquitinating enzymes (DUBs), plays a role in regulating germ cell apoptosis and the differentiation of spermatocytes into sperm cells [25,26]
Twenty-five instances of positive selection were identified in 15 genes from the laurasiatherian dataset using the free-ratio model
Summary
The testis, the organ in which spermatogenesis begins, is important for male reproduction. The abdominal testicular mammals have testes remaining in the urogenital ridge near the kidneys, showing no testicular descent (e.g., most afrotherians) or just descending into the lower abdomen, like dolphins and seals [6,8,9] These abdominal testicular mammals can undergo normal spermatogenesis and maintain healthy reproduction functions, unlike scrotal testicular mammals that suffer from “cryptorchidism injury”. UBA1/UBE1, an E1, initiates the cascade of UPS and is involved in male reproduction via spermatogenesis [20]; UBE2A/HR6A, an E2, is required for the maintenance of X chromosome silencing in spermatocytes and spermatids [21]; RNF8, an E3, participates in sperm cell nucleosome remodeling through the ubiquitination of histones [22,23]; PSMA8, a testis-specific 20S core proteasome subunit, degrades pro-meiotic I protein during spermatogenesis [24]; UCHL3, a DUB, plays a role in regulating germ cell apoptosis and the differentiation of spermatocytes into sperm cells [25,26]. Positive selection, accelerated evolution and convergent evolution of spermatogenesisrelated UPS genes, together with functional evidence of RNF8, provided some new insights into the reproductive adaptation in abdominal testicular mammals
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