Abstract
BackgroundThe 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.ResultsWe 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.ConclusionsOur 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.
Highlights
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
Some other hypotheses have been raised to explain the evolutionary origin of testicular descent and the function of the scrotum—e.g. the ‘training hypothesis’ argues that the scrotum exposes the sperm to a hostile environment to “train” it for further fertilization [7], Portmann [8] contends that the scrotum serves as a sexual signal in some mammals, and the ‘galloping hypothesis’ states that the scrotum originated in mammals that gallop or jump and protects spermatogenesis and sperm storage from consequent fluctuations in intra-abdominal pressure [9, 10]
Molecular evolution of cryptorchidism‐related genes involved in testicular descent Branch model analysis in PAML detected 36 genes that evolved significantly increased molecular substitution rates in ascrotal incompletely descended testes (IDT) and undescended testes (UDT) branches compared to completely descended testes (CDT) species (Fig. 2 and Additional file 1: Table S3)
Summary
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. The testis is a consequential male exocrine gland that produces spermatozoa and an endocrine gland that secretes sex hormones. For most mammals, both the testis and epididymis are located in the scrotum, which is outside of the body and protects the testis. The. Chai et al BMC Ecol Evo (2021) 21:22 multi-version ‘cooling hypothesis’ [1, 2] suggests that the scrotum provides an environment 2–4 °C cooler than the normal body temperature; germinal epithelium and spermatozoa are acutely sensitive to heat [3], so this environment is optimal for spermatogenesis and sperm storage [4,5,6]. Cryptorchidism, a congenital malformation in most mammals, can affect normal male physiological functions
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