Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location

Zeng, Yu; Lou, Shang Ling; Liao, Wen Bo; Jehle, Robert

doi:10.1186/1471-2148-14-104

Cited by 35 publications

(46 citation statements)

References 62 publications

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“…; Zeng et al. ). However, we extended these results by also showing positive selection on sperm numbers and, importantly, how both traits jointly ( m * s * and m */ s *) respond to selection.…”

Section: Discussionmentioning

confidence: 98%

“…; Anstis ; Zeng et al. ). In the fishes, we recorded the egg deposition site (into nest, onto plants/rocks, into open water/scattering over substrate), water movement (stagnant, flowing/turbulent), and the mating system (pair spawning, pair spawning with additional males, group spawning), primarily based on Teletchea et al.…”

Section: Methodsmentioning

confidence: 99%

“…; Zeng et al. ), but to our knowledge, how sperm size and number vary relative to one another in the context of Parker et al.’s () gamete investment models has not been explored in either taxon. Joint examination of these ejaculate traits, however, is critical due to their nonindependent evolution.…”

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confidence: 99%

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Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

et al. 2017

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The evolution of sperm quality and quantity is shaped by various selective processes, with sperm competition generally considered the primary selective agent. Particularly in external fertilizers, however, sperm limitation through gamete dispersal can also influence gamete investments, but empirical data examining this effect are limited. Here, we studied the relative importance of sperm competition and the spawning conditions in explaining the macroevolutionary patterns of sperm size and number within two taxa with external fertilization but differences in their reproductive biology. In frogs, sperm swim slowly but for up to hours as they penetrate the gelatinous egg coating, whereas fish sperm typically swim fast, are very short-lived (seconds to minutes), and often face a relatively higher risk of being moved away from the ova by currents. Our phylogenetic models and path analyses revealed different trajectories of ejaculate evolution in these two taxa. Sperm size and number responded primarily to variation in sperm competition in the anurans, but more strongly to egg number and water turbulence in the fishes. Whereas the results across anurans align with the general expectation that sexual selection is the main driver of ejaculate evolution, our findings across the fishes suggest that sperm limitation has been underappreciated. K E Y W O R D S :Anurans, fishes, reproductive investment, sperm number, sperm length, sperm size-number trade-off.

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Section: Discussionmentioning

confidence: 98%

Section: Methodsmentioning

confidence: 99%

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Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

et al. 2017

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“…Following Byrne et al (2002) and Zeng et al (2014), we used the mating system as an imperfect surrogate for the level of sperm competition at two factorial levels (Table S1): simultaneous polyandry (multimale amplexus and simultaneous sperm release, resulting in sperm competition) and monandry (females mate with one male over the course of a breeding season and deposit a single clutch). Additionally, we obtained for each species information on two main types of reproduction, explosive and prolonged breeding, from Fei et al (2010).…”

Section: Sample Collection and Preparationmentioning

confidence: 99%

Population density and structure drive differential investment in pre- and postmating sexual traits in frogs

2017

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Sexual selection theory predicts a trade-off between premating (ornaments and armaments) and postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is costly and that total reproductive investments are limited. The number of males in competition, the reproductive gains from investing in premating sexual traits, and the level of sperm competition are all predicted to influence how males allocate their finite resources to these traits. Yet, empirical examination of these predictions is currently scarce. Here, we studied relative expenditure on pre- and postmating sexual traits among frog species varying in their population density, operational sex ratio, and the number of competing males for each clutch of eggs. We found that the intensifying struggle to monopolize fertilizations as more and more males clasp the same female to fertilize her eggs shifts male reproductive investment toward sperm production and away from male weaponry. This shift, which is mediated by population density and the associated level of male-male competition, likely also explains the trade-off between pre- and postmating sexual traits in our much broader sample of anuran species. Our results highlight the power of such a multilevel approach in resolving the evolution of traits and allocation trade-offs.

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“…However, the evolution of sperm has to be viewed within the constraints of the selective environment, as selection is likely to favor those sperm that survive and compete best under their specific environmental conditions. Compared to internal fertilizers, in which sperm evolution is greatly affected by the female reproductive tract (Briskie et al 1997;Pitnick et al 1999;Immler et al 2011;Lüpold and Fitzpatrick 2015), extrinsic environmental stressors (e.g., temperature, pH, osmolality) or spawning conditions (e.g., sperm release into water column versus foam nests) can play important roles in external fertilizers (Morisawa et al 1983;Billard et al 1986;Byrne et al 2003;Zeng et al 2014). Additionally, ejaculate-quality traits can be sensitive to the environmental conditions, including sperm length that can change significantly in ectothermic species even at a slight alteration of ambient temperature experienced by males during development or as adults (Blanckenhorn and Hellriegel 2002;Adriaenssens et al 2012;Breckels and Neff 2013;Minoretti et al 2013;Vasudeva et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

Jin

Yang

Liao

et al. 2016

Behav Ecol Sociobiol

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There is substantial comparative and growing experimental evidence that the competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, less is known about the extent of natural variation in these investments relative to environmental variables affecting resource availability and mating system dynamics, which would allow insights into the mechanisms shaping reproductive allocation. Here, we studied interpopulation variation in male investments in testis size and sperm length across 25 populations of the Asian grass frog Fejervarya limnocharis along a 1550-km latitudinal and 1403-m altitudinal transect in China. We found relative testis mass and sperm length, male somatic condition, and the male/female sex ratio to increase with elevation but not latitude or longitude. Our results suggest that environmental variation may underlie local adaptations to reproductive investments among natural populations, mediated by differences in the availability of both resources and sexual partners (including the resulting male-male competition). These findings contrast with previous predictions that increasing latitude and/or elevation should lead to declining reproductive investments in male anurans due to shortening breeding seasons, declining resource availability, and lowering (rather than increasing) male/female sex ratios. We discuss these species differences in the context of differential resource allocation strategies, breeding ecology, and patterns of male-male competition. These differences show the need for future work on reproductive investments in anurans beyond the few model systems and for potential extension of the theoretical framework to species with different mating systems and strategies. Significance statementDespite a broad theoretical framework of how environmental parameters can shape mating systems and these, in turn, drive the evolution of reproductive traits, there is limited empirical evidence from natural populations. We examined differences in the size of testes and sperm between males between natural populations along latitudinal and altitudinal transects. We found that at high elevation, males were relatively heavier and had longer sperm and disproportionately large testes, and the sex ratio was more male-biased. These interpopulation differences may reflect local adaptations to variation in the resource availability and temporal patterns of female availability, which affects the breeding synchrony, sperm demand, and male-male competition for mates and paternity. However, our results differ from previous studies of frogs, possibly due to different breeding ecology, which highlights the need for further work and potential extension of theoretical predictions to non-model anurans.

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Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location

Cited by 35 publications

References 62 publications

Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

Population density and structure drive differential investment in pre- and postmating sexual traits in frogs

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

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