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

Kopania, Emily E. K.; Thomas, Gregg W. C.; Hutter, Carl R.; Mortimer, Sebastian M. E.; Callahan, Colin M.; Roycroft, Emily; Achmadi, Anang S.; Breed, William G.; Clark, Nathan L.; Esselstyn, Jacob A.; Rowe, Kevin C.; Good, Jeffrey M.

doi:10.1101/2023.08.30.555585

“…Alternatively, selection against hybridization in zones of sympatry may have driven reproductive character displacement, contributing to speciation. Diversifying selection on genes involved in sperm morphology and spermatogenesis across broader murine rodents provides further evidence for the role of sperm morphology in speciation (Kopania et al., 2023; Roycroft, Achmadi, et al., 2021). In addition, chromosomal rearrangements (identified via C‐ and G‐banding) are evident across all six species examined here, including at least one additional pericentric inversion on chromosome 9 differentiating P. pilbarensis sp.…”

Section: Discussionmentioning

confidence: 98%

Speciation across biomes: Rapid diversification with reproductive isolation in the Australian delicate mice

Roycroft,

Ford,

Ramm

et al. 2024

Molecular Ecology

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Phylogeographic studies of continental clades, especially when combined with palaeoclimate modelling, provide powerful insight into how environment drives speciation across climatic contexts. Australia, a continent characterized by disparate modern biomes and dynamic climate change, provides diverse opportunity to reconstruct the impact of past and present environments on diversification. Here, we use genomic‐scale data (1310 exons and whole mitogenomes from 111 samples) to investigate Pleistocene diversification, cryptic diversity, and secondary contact in the Australian delicate mice (Hydromyini: Pseudomys), a recent radiation spanning almost all Australian environments. Across northern Australia, we find no evidence for introgression between cryptic lineages within Pseudomys delicatulus sensu lato, with palaeoclimate models supporting contraction and expansion of suitable habitat since the last glacial maximum. Despite multiple contact zones, we also find little evidence of introgression at a continental scale, with the exception of a potential hybrid zone in the mesic biome. In the arid zone, combined insights from genetic data and palaeomodels support a recent expansion in the arid specialist P. hermannsburgensis and contraction in the semi‐arid P. bolami. In the face of repeated secondary contact, differences in sperm morphology and chromosomal rearrangements are potential mechanisms that maintain species boundaries in these recently diverged species. Additionally, we describe the western delicate mouse as a new species and recommend taxonomic reinstatement of the eastern delicate mouse. Overall, we show that speciation in an evolutionarily young and widespread clade has been driven by environmental change, and potentially maintained by divergence in reproductive morphology and chromosome rearrangements.

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“…Despite relatively high mating success among dominant males, some elephant seal males have lower-than-expected reproductive success, possibly related to reduced male fertility (Hoelzel et al, 1999). Reduced sperm competition in Old World mice and rats (Murinae) is associated with the evolution of smaller testis mass, sperm morphologies, and signals of relaxed purifying selection on protein-coding genes expressed in the late stages of spermatogenesis and seminal vesicles (Kopania et al, 2023; Murat et al, 2023). These results are consistent not only with our observations in gorilla, but also with studies of other mouse lineages (Good and Nachman, 2005; Kopania et al, 2022), a broad selection of mammals (Murat et al, 2023), and even among promiscuous Tanganyikan cichlids ( Ophthalmotilapia ventralis ) (Morita et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Pervasive relaxed selection on spermatogenesis genes coincident with the evolution of polygyny in gorillas

Bowman,

Silva,

Schüftan

et al. 2023

Preprint

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Gorillas have a polygynous social system in which the highest-ranking male has almost exclusive access to females and sires most of the offspring in the troop. Such behavior results in a dramatic reduction of sperm competition, which is ultimately associated with numerous traits that cause low efficacy of gorilla spermatogenesis. However, the molecular basis behind the remarkable erosion of the gorilla male reproductive system remains unknown. Here, we explored the genetic consequences of the polygynous social system in gorillas by testing for altered selection intensity across 13,310 orthologous protein-coding genes from 261 Eutherian mammals. We identified 578 genes with relaxed purifying selection in the gorilla lineage, compared with only 96 that were positively selected. Genes under relaxed purifying selection in gorillas have accumulated numerous deleterious amino acid substitutions, their expression is biased towards male germ cells, and are enriched in functions related to meiosis and sperm biology. We tested the function of gorilla relaxed genes previously not implicated in sperm biology using the Drosophila model system and identified 41 novel spermatogenesis genes required for normal fertility. Furthermore, by exploring exome/genome sequencing data of infertile men with severe spermatogenic impairment, we found that the human orthologs of the gorilla relaxed genes are enriched for loss-of-function variants in infertile men. These data provide compelling evidence that reduced sperm competition in gorillas is associated with relaxed purifying selection on genes related to male reproductive function. The accumulation of deleterious mutations in these genes likely provides the mechanistic basis behind the low efficacy of gorilla spermatogenesis and uncovers new candidate genes for human male infertility.

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Pervasive relaxed selection on spermatogenesis genes coincident with the evolution of polygyny in gorillas

Bowman,

Silva,

Schüftan

et al. 2024

Preprint

1

0

View full text Add to dashboard Cite

Gorillas have a polygynous social system in which the highest-ranking male has almost exclusive access to females and sires most of the offspring in the troop. Such behavior results in a dramatic reduction of sperm competition, which is ultimately associated with numerous traits that cause low efficacy of gorilla spermatogenesis. However, the molecular basis behind the remarkable erosion of the gorilla male reproductive system remains unknown. Here, we explored the genetic consequences of the polygynous social system in gorillas by testing for altered selection intensity across 13,310 orthologous protein-coding genes from 261 Eutherian mammals. We identified 578 genes with relaxed purifying selection in the gorilla lineage, compared with only 96 that were positively selected. Genes under relaxed purifying selection in gorillas have accumulated numerous deleterious amino acid substitutions, their expression is biased towards male germ cells, and are enriched in functions related to meiosis and sperm biology. We tested the function of gorilla relaxed genes previously not implicated in sperm biology using the Drosophila model system and identified 41 novel spermatogenesis genes required for normal fertility. Furthermore, by exploring exome/genome sequencing data of infertile men with severe spermatogenic impairment, we found that the human orthologs of the gorilla relaxed genes are enriched for loss-of-function variants in infertile men. These data provide compelling evidence that reduced sperm competition in gorillas is associated with relaxed purifying selection on genes related to male reproductive function. The accumulation of deleterious mutations in these genes likely provides the mechanistic basis behind the low efficacy of gorilla spermatogenesis and uncovers new candidate genes for human male infertility.

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

Cited by 4 publications

References 142 publications

Speciation across biomes: Rapid diversification with reproductive isolation in the Australian delicate mice

Speciation across biomes: Rapid diversification with reproductive isolation in the Australian delicate mice

Pervasive relaxed selection on spermatogenesis genes coincident with the evolution of polygyny in gorillas

Pervasive relaxed selection on spermatogenesis genes coincident with the evolution of polygyny in gorillas

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