Morphological diversity of the spermatozoon and male reproductive tract in Australian Hopping mice, genus Notomys – is it determined by sexual selection?

Abstract

Hopping mice (Genus Notomys) are a monophyletic group of Australian Old Endemic murid rodents in the Tribe Hydromyini four of which, Notomys alexis, N. mitchellii, N. fuscus and N cervinus, occur in arid or semiarid environments. Here, we compare the size and morphology of their testes, spermatozoa, accessory sex glands and external genitalia across the species, and from these data, we draw conclusions as to their likely breeding systems. We show that both wild caught and laboratory bred adult N. alexis, N. fuscus and N. mitchellii individuals have extremely small testes, but their spermatozoa vary in morphology across the species. The ventral prostate is the only large accessory sex gland present, and their glans penis has very large spines. By contrast N. cervinus individuals have significantly larger testes with their spermatozoa being less variable but generally more complex in morphology, their seminal vesicles and coagulating glands are much larger, whereas the glans penis has only small spines. Since these reproductive traits in N. cervinus are more similar to those of most other hydromyine rodents in the genus Pseudomys, they are likely to reflect the retention of the ancestral condition within the Notomys lineage whereas the divergent reproductive traits of the other species of tiny testes, variable sperm, small seminal vesicles and coagulating glands and large penile spines are probably more recently derived traits. It is suggested that N. cervinus with its relatively larger testes mass and greater abundance of sperm of more consistent morphology has retained a mating system that may potentially involve some intermale sperm competition whereas, by contrast, the reproductive anatomy of the other three Notomys species suggests that these species exhibit monogamy.

Sperm competition intensity shapes divergence in both sperm morphology and reproductive genes across murine rodents

“…For example, there is a negative correlation between intraspecific variation in sperm morphology and relative testes mass in rodents and passerine birds, suggesting that sperm competition pressures may reduce variation in sperm morphology (58, 74). In the small testes murine species Notomys alexis and N. fuscus , there is high intraspecific variation in sperm hook morphology, with some having small hooks or ventral processes and others lacking these structures altogether (75). Thus, sperm competition may impose purifying selection on genes involved in sperm development to facilitate a higher proportion of high-quality sperm in the ejaculate.…”

Apical Sperm Hook Morphology Is Linked to Sperm Swimming Performance and Sperm Aggregation in Peromyscus Mice

“…We verified that relative testes size did not differ in these males between males with normal and abnormal sperm, but we found that males that produced sperm with abnormal hook phenotypes had significantly lower caudal epididymal sperm counts, suggesting reduced sperm production efficiency. An examination of sperm within Australian Hopping mice revealed a shortening or absence of the apical hook and simplification of the sperm head morphology within two species, which the authors considered to be a recently derived trait and suggest it may be due to a monogamous mating system due to relaxed levels of sperm competition [ 8 ]. Importantly, discovering the subset of males in our study with abnormally hooked or hookless sperm, we confirmed that several of these males who had been paired with a female had produced litters.…”

“…In Eutherian mammals, sperm typically feature a round, paddle-shaped and symmetrical sperm head, but several lineages of muroid rodent species have independently evolved sperm cells with a falciform apical hook—a cytoskeletal structure extending from the sperm head that is composed of acrosomal material [ 3 , 4 , 5 , 6 ]. A few rare species lack sperm hooks entirely [ 3 , 4 , 6 , 7 , 8 ], whereas some possess multiple sperm hooks [ 8 , 9 , 10 , 11 ]. For those species that do possess a sperm hook, its size, shape, and position is highly variable across species [ 3 , 5 , 12 ].…”