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Sperm competition and fertilization mode in fishes.

ABSTRACT: Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue 'Fifty years of sperm competition'.

SUBMITTER: Fitzpatrick JL

PROVIDER: S-EPMC7661453 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Sperm competition and fertilization mode in fishes.

Fitzpatrick John L JL

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20201019 1813

Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examinat ...[more]

PMID: 33070731

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Project description:Fertilization mode may affect sperm characteristics, such as morphology, velocity, and motility. However, there is little information on how fertilization mode affects sperm evolution because several factors (e.g., sperm competition) are intricately intertwined when phylogenetically distant species are compared. Here, we investigated sperm characteristics by comparing seven externally and four internally fertilizing marine fishes from three different groups containing close relatives, considering sperm competition levels. The sperm head was significantly slenderer in internal fertilizers than in external fertilizers, suggesting that a slender head is advantageous for swimming in viscous ovarian fluid or in narrow spaces of the ovary. In addition, sperm motility differed between external and internal fertilizers; sperm of external fertilizers were only motile in seawater, whereas sperm of internal fertilizers were only motile in an isotonic solution. These results suggest that sperm motility was adapted according to fertilization mode. By contrast, total sperm length and sperm velocity were not associated with fertilization mode, perhaps because of the different levels of sperm competition. Relative testis mass (an index of sperm competition level) was positively correlated with sperm velocity and negatively correlated with the ratio of sperm head length to total sperm length. These findings suggest that species with higher levels of sperm competition have faster sperm with longer flagella relative to the head length. These results contradict the previous assumption that the evolution of internal fertilization increases the total sperm length. In addition, copulatory behavior with internal insemination may involve a large genital morphology, but this is not essential in fish, suggesting the existence of various sperm transfer methods. Although the power of our analyses is not strong because of the limited number of species, we propose a new scenario of sperm evolution in which internal fertilization would increase sperm head length, but not total sperm length, and change sperm motility.

Project description:Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An "overall sperm quality" parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert.

Project description:Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female's ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa.

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Sperm competition and fertilization mode in fishes.

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Sperm competition and fertilization mode in fishes.

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