Postcopulatory Sexual Selection Increases Atp Content in Rodent Spermatozoa

Tourmente, Maximiliano; Rowe, Melissah; González-Barroso, M. Mar; Rial, Eduardo; Gomendio, Montserrat; Roldán, Eduardo R. S.

doi:10.1111/evo.12079

Cited by 55 publications

(83 citation statements)

References 68 publications

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“…The higher prevalence of sperm DNA fragmentation in species with high levels of sperm competition could be due to higher levels of oxidative stress in these species. Recently, it has been shown that the increase in sperm swimming velocity observed in rodent species that experience high levels of sperm competition is driven to a great extent by a rise in the content of sperm ATP [20,34,46]. That is, in species with high levels of sperm competition there seem to be metabolic changes and an increase in metabolism that allow sperm cells to swim faster [47].…”

Section: Discussionmentioning

confidence: 99%

“…Such reduced baseline levels and higher protection against DNA damage can be attained, for example, by increasing antioxidant measures in the male reproductive tract, seminal fluid and spermatozoa themselves. On the other hand, the increased metabolism needed to fuel higher sperm swimming velocity in species that experience high levels of sperm competition [20] could lead to a marked rise in the production of reactive oxygen species (ROS) within sperm cells, resulting in a net loss in DNA integrity, despite countermeasures evolved to prevent or repair such damage. In addition, the faster rates of spermatogenesis in species with high levels of sperm competition [3] may result in less controlled DNA condensation and packaging of DNA leading to higher incidences of DNA fragmentation.…”

Section: Introductionmentioning

confidence: 99%

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A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

et al. 2016

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Sperm competition, a prevalent evolutionary process in which the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects on DNA integrity. Sperm DNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of sperm competition using the sperm chromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in noncapacitating and capacitating conditions resulted in only a small increase in sperm DNA damage. Importantly, levels of sperm competition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

et al. 2016

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“…This may be realized by an increase of sperm producing tissue within the testis as observed in birds [72]. Additionally, also ejaculate quality may be increased, but in rodents such sperm competition metrics are typically strongly related to RTS [73][74][75][76].…”

Section: Discussionmentioning

confidence: 99%

Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species

Klemme

Soulsbury

Henttonen³

2014

Proc. R. Soc. B.

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Across species, there is usually a positive relationship between sperm competition level and male reproductive effort on ejaculates, typically measured using relative testes size (RTS). Within populations, demographic and ecological processes may drastically alter the level of sperm competition and thus, potentially affect the evolution of testes size. Here, we use longitudinal records (across 38 years) from wild sympatric Fennoscandian populations of five species of voles to investigate whether RTS responds to natural fluctuations in population density, i.e. variation in sperm competition risk. We show that for some species RTS increases with density. However, our results also show that this relationship can be reversed in populations with large-scale between-year differences in density. Multiple mechanisms are suggested to explain the negative RTS-density relationship, including testes size response to density-dependent species interactions, an evolutionary response to sperm competition levels that is lagged when density fluctuations are over a certain threshold, or differing investment in pre-and post-copulatory competition at different densities. The results emphasize that our understanding of sperm competition in fluctuating environments is still very limited.

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“…Since larger cells might contain greater quantities of ATP due to increased internal volume, differences in cell size should be taken into account when testing for possible differences in sperm ATP concentration. Since data on sperm volume is scarce and relatively difficult to obtain for mammals [46,47], and in cylindrically-shaped objects volume is proportional to length, we calculated the "length-adjusted ATP concentration" (amol μm ) as the ratio between the amount of ATP per sperm for each species and its total sperm length [48]. Thus, we performed simple linear regression using ATP amount per sperm and length-adjusted ATP concentration as dependent variables and the mass-specific metabolic rate as predictor in order to assess the effect of the mass-specific metabolic rate on the absolute and length-proportional amount of ATP per sperm.…”

Section: Discussionmentioning

confidence: 99%

“…Sperm velocity has been reported to be linked to sperm ATP content and concentration in muroid rodents, in which increased sperm ATP content seems to be promoted by an increase of the sperm competition level [48]. A previous study on the influence of metabolic rate on sperm quality in mammals found a positive association the between mass-specific metabolic Phylogenetically controlled multiple regression analyses (PGLS).…”

Section: Discussionmentioning

confidence: 99%

Mass-specific metabolic rate influences sperm performance through energy production in mammals

Tourmente

Roldán

2014

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Mass-specific metabolic rate, the rate at which organisms consume energy per gram of body weight, is negatively associated with body size in metazoans. As a consequence, small species have higher cellular metabolic rates and are able to process resources at a faster rate than large species. Since mass-specific metabolic rate has been shown to constrain evolution of sperm traits, and most of the metabolic activity of sperm cells relates to ATP production for sperm motility, we hypothesized that mass-specific metabolic rate could influence sperm energetic metabolism at the cellular level if sperm cells maintain the metabolic rate of organisms that generate them. We compared data on sperm straight-line velocity, mass-specific metabolic rate, and sperm ATP content from 40 mammalian species and found that the mass-specific metabolic rate positively influences sperm swimming velocity by (a) an indirect effect of sperm as the result of an increased sperm length, and (b) a direct effect independent of sperm length. In addition, our analyses show that species with higher mass-specific metabolic rate have higher ATP content per sperm and higher concentration of ATP per μm of sperm length, which are positively associated with sperm velocity. In conclusion, our results suggest that species with high mass-specific metabolic rate have been able to evolve both long and fast sperm. Moreover, independently of its effect on the production of larger sperm, the mass-specific metabolic rate is able to influence sperm velocity by increasing sperm ATP content in mammals.

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Postcopulatory Sexual Selection Increases Atp Content in Rodent Spermatozoa

Cited by 55 publications

References 68 publications

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species

Mass-specific metabolic rate influences sperm performance through energy production in mammals

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