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1. Sperm Cyst “Looping”: A Developmental Novelty Enabling Extreme Male Ornament Evolution

   https://doi.org/https://doi.org/10.3390/cells10102762  

   Zeeshan A. Syed 1, * (October 2021, Cells)

   null (Ed.)

   Abstract: Postcopulatory sexual selection is credited as a principal force behind the rapid evolution of reproductive characters, often generating a pattern of correlated evolution between interacting, sex-specific traits. Because the female reproductive tract is the selective environment for sperm, one taxonomically widespread example of this pattern is the co-diversification of sperm length and female sperm-storage organ dimension. In Drosophila, having testes that are longer than the sperm they manufacture was believed to be a universal physiological constraint. Further, the energetic and time costs of developing long testes have been credited with underlying the steep evolutionary allometry of sperm length and constraining sperm length evolution in Drosophila. Here, we report on the discovery of a novel spermatogenic mechanism—sperm cyst looping—that enables males to produce relatively long sperm in short testis. This phenomenon (restricted to members of the saltans and willistoni species groups) begins early during spermatogenesis and is potentially attributable to heterochronic evolution, resulting in growth asynchrony between spermatid tails and the surrounding spermatid and somatic cyst cell membranes. By removing the allometric constraint on sperm length, this evolutionary innovation appears to have enabled males to evolve extremely long sperm for their body mass while evading delays in reproductive maturation time. On the other hand, sperm cyst looping was found to exact a cost by requiring greater total energetic investment in testes and a pronounced reduction in male lifespan. We speculate on the ecological selection pressures underlying the evolutionary origin and maintenance of this unique adaptation. 

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2. Sperm length and seminal fluid proteins promote male reproductive success in Drosophila melanogaster

   https://doi.org/10.1093/jeb/voaf065  

   Galvin, Jake; Yedigarian, Sevan; Rahman, Mohammad; Borziak, Kirill; DeNieu, Michael; Larson, Erica L; Manier, Mollie K (April 2025, Journal of Evolutionary Biology)

   Bilde, Trine; Rowe, Melissah (Ed.)

   Abstract Spermatozoal morphology varies widely within and among species, often corresponding to the shape of the female sperm storage organs in ways that can impact fertilization. To understand genetic mechanisms of sperm length variation, we compared gene expression patterns in the testes of Drosophila melanogaster males that produce either long or short sperm. We found that genes upregulated in long sperm testes are enriched for long noncoding RNAs and seminal fluid proteins (Sfps). Transferred to the female during mating, Sfps are secreted by the male accessory glands and affect female remating rate, physiology, and behavior. While sperm and Sfps are both critical for male reproductive success, they are largely considered to be functionally and genetically independent, and Sfps have no known function in testes. Knockouts of two Sfps upregulated in long sperm males, Sex Peptide and ovulin, resulted in shorter sperm, suggesting Sfps may contribute to sperm length development. Consistent with this, knockout of accessory gland function did not affect sperm length, indicating accessory gland expression had no influence on spermatogenesis. We also found that long sperm males were better able to delay female remating, suggesting a dual advantage in sperm competition by both delaying female remating and resisting sperm displacement. However, we found that the delay in female remating does not necessarily increase progeny or paternity success. Thus, multiple components of the ejaculate promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain. 

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3. Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males

   https://doi.org/10.3390/cells10102612  

   Alonzo, Suzanne H.; Stiver, Kelly A.; Kindsvater, Holly K.; Marsh-Rollo, Susan E.; Nugent, Bridget; Kazancıoğlu, Erem (October 2021, Cells)

   Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only “sneak” spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production. 

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

   https://doi.org/10.1093/evolut/qpae146  

   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; et al (October 2024, Evolution)

   Abstract It remains unclear how variation in the intensity of sperm competition shapes phenotypic and molecular evolution across clades. Mice and rats in the subfamily Murinae are a rapid radiation exhibiting incredible diversity in sperm morphology and production. We combined phenotypic and genomic data to perform phylogenetic comparisons of male reproductive traits and genes across 78 murine species. We identified several shifts towards smaller relative testes mass (RTM), presumably reflecting reduced sperm competition. Several sperm traits were associated with RTM, suggesting that mating system evolution selects for convergent suites of traits related to sperm competitive ability. We predicted that sperm competition would also drive more rapid molecular divergence in species with large testes. Contrary to this, we found that many spermatogenesis genes evolved more rapidly in species with smaller RTM due to relaxed purifying selection. While some reproductive genes evolved rapidly under recurrent positive selection, relaxed selection played a greater role in underlying rapid evolution in small testes species. Our work demonstrates that postcopulatory sexual selection can impose strong purifying selection shaping the evolution of male reproduction and that broad patterns of molecular evolution may help identify genes that contribute to male fertility. 

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5. An experimental test of the evolutionary consequences of sympatry in Drosophila subquinaria

   https://doi.org/10.1093/evolut/qpad236  

   Jarvis, Will_M C; Arthur, Nicholas J; Rundle, Howard D; Dyer, Kelly A (December 2023, Evolution)

   Huang, Jen-Pan; Connallon, Tim (Ed.)

   Prezygotic isolation is often stronger between sympatric as opposed to allopatric taxa, but the underlying cause can be difficult to infer from comparative studies alone. Experimental evolution, where evolutionary responses to treatments manipulating the presence/absence of heterospecific individuals are tracked, can provide a powerful complementary approach. We used experimental evolution to investigate a naturally occurring pattern of reproductive character displacement in the mushroom-feeding fly, Drosophila subquinaria. In nature, female D. subquinaria from populations sympatric with the closely related Drosophila recens discriminate more strongly against heterospecific males than do females from allopatric populations. Starting with 16 replicate allopatric populations of D. subquinaria, we manipulated the presence/absence of D. recens during mating (experimental sympatry vs. control) and, when present, we allowed hybrids to live or kill them each generation. Across 12 generations, heterospecific offspring production from no-choice mating trials between D. subquinaria females and D. recens males declined in both experimental sympatry treatments relative to the control, suggesting increased sexual isolation. Male cuticular hydrocarbon profiles also evolved, but only in the hybrids killed treatment. Our results strongly imply that the existing reproductive character displacement in wild D. subquinaria populations was an evolutionary response to selection arising from secondary contact with D. recens. 

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