The effects of male social environment on sperm phenotype and genome integrity

Silva, Willian T. A. F.; Sáez‐Espinosa, Paula; Torijo‐Boix, Stéphanie; Romero, Alejandro; Devaux, Caroline; Durieux, Mathilde; Gómez‐Torres, María José; Immler, Simone

doi:10.1111/jeb.13435

Cited by 22 publications

(25 citation statements)

References 65 publications

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“…Moreover, a recent study of zebrafish found that males exposed to rivals had sperm with morphologies that are predicted to promote more efficient fertilization but also had greater levels of DNA damage compared to the sperm of males that were not exposed to rivals, supporting the notion of a trade‐off between male expenditure on gaining fertilizations and on the genetic quality of the offspring they sire (Silva et al. ).…”

Section: Discussionmentioning

confidence: 90%

Nongenetic paternal effects via seminal fluid

Simmons

Lovegrove

2019

Evolution Letters

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Mounting evidence suggests that nongenetic paternal effects on offspring may be widespread among animal taxa, but the mechanisms underlying this form of nongenetic inheritance are not yet fully understood. Here, we show that seminal fluids underlie paternal effects on early offspring survival in an insect, the cricket Teleogryllus oceanicus, and quantify the contribution of this paternal effect to the inheritance of this important fitness trait. We used castrated males within a full‐sib half‐sib experimental design to show that seminal fluid donors were responsible for variation in the survival of developing embryos to hatching, and in their subsequent survival to adulthood. Increased expression of two seminal fluid protein genes, previously found to be positively associated with sperm quality, was found to be negatively associated with embryo survival. These nongenetic paternal effects hold important implications for the evolution of adaptive maternal responses to sperm competition, and more broadly for the interpretation of sire effects from classic quantitative genetic breeding designs.

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Section: Discussionmentioning

confidence: 90%

Nongenetic paternal effects via seminal fluid

Simmons

Lovegrove

2019

Evolution Letters

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“…The differences in sperm longevity we found among males (indicated by the male effect in the main model, see table 1) may reflect a differential investment according to the male social environment. Earlier studies in the zebrafish showed that sperm traits vary with the intensity of male-male competition and male social status and affect the survival and performance of the resulting offspring (Zajitschek et al 2014;Zajitschek et al 2017), possibly due to the higher mutational load in sperm of stressed males (Silva et al 2019). In addition, longer-lived sperm selected within ejaculates sire embryos with higher survival and adult fitness in zebrafish (Alavioon et al 2019) (Darszon et al 2004) and in several species of externally fertilizing fish (Yanagimachi et al 1992).…”

Section: Discussionmentioning

confidence: 99%

Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish

2019

Self Cite

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In polyandrous mating systems, females maintain the opportunity to bias male fertilization success after mating in a process known as cryptic female choice. Mechanisms of cryptic female choice have been described both in internal and external fertilizers, and may affect fertilization processes at different stages before, during, and after fertilization. In internal fertilizers, females have substantial control over sperm storage and fertilization, whereas in external fertilizers, female control is limited. A key factor proposed to mediate cryptic female choice is the fluid surrounding the eggs, the ovarian fluid, as it may directly affect sperm performance. Here, we studied the role of ovarian fluid in post-mating sexual selection using the zebrafish, Danio rerio. Firstly, we assessed how ovarian fluid affects sperm swimming performance compared with freshwater. We focused on sperm motility, velocity, swimming trajectory, and longevity, all traits associated with competitive fertilization success in externally fertilizing fish. In a second step, we used a North Carolina II design to explore female, male, and female x male effects by testing sperm motility of 2 males in the ovarian fluid of 2 females in a total of 11 blocks. Our results indicate that the ovarian fluid affects sperm performance differently from freshwater. Specifically, sperm velocity, motility, and longevity were higher in the ovarian fluid than in freshwater, whereas sperm linearity and beat cross frequency showed the opposite pattern. Moreover, these effects varied according to male, female, and male x female identities, supporting the potential for cryptic female choice mediated by ovarian fluid in this species.

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“…Furthermore, germline and sperm cells are particularly well protected from oxidative damage in guppies, as suggested by the relatively low senescence rate of ejaculate quality in this species (Gasparini, Devigili, & Pilastro, 2019). However, in the zebrafish Danio rerio , a high male–male competition environment leads males to produce faster swimming sperm, at a cost of DNA integrity and offspring fitness (Silva et al., 2019; Zajitschek, Hotzy, Zajitschek, & Immler, 2014), suggesting that this protection is incomplete. To distinguish between these alternative explanations, it would be necessary to experimentally manipulate male courtship effort independently from sperm priming.…”

Section: Discussionmentioning

confidence: 99%

Female sperm storage mediates post‐copulatory costs and benefits of ejaculate anticipatory plasticity in the guppy

Cardozo

Devigili

Antonelli

et al. 2020

J of Evolutionary Biology

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Males of many species evolved the capability of adjusting their ejaculate phenotype in response to social cues to match the expected mating conditions. When females store sperm for a prolonged time, the expected fitness return of plastic adjustments of ejaculate phenotype may depend on the interval between mating and fertilization. Although prolonged female sperm storage (FSS) increases the opportunity for sperm competition, as a consequence of the longer temporal overlap of ejaculates from several males, it may also create variable selective forces on ejaculate phenotype, for example by exposing trade‐offs between sperm velocity and sperm survival. We evaluated the relationship between the plasticity of ejaculate quality and FSS in the guppy, Poecilia reticulata, a polyandrous live‐bearing fish in which females store sperm for several months and where stored sperm contribute significantly to a male's lifelong reproductive success. In this species, males respond to the perception of future mating opportunities by increasing the quantity (number) and quality (swimming velocity) of ready‐to‐use sperm (an anticipatory response called ‘sperm priming’). Here we investigated (a) the effect of sperm priming on in vitro sperm viability at stripping and its temporal decline (as an estimate of sperm survival), and (b) the in vivo competitive fertilization success in relation to female sperm storage using artificial insemination. As expected, sperm‐primed males produced more numerous and faster sperm, but with a reduced in vitro sperm viability at stripping and after 4 hr, compared with their counterparts. Artificial insemination revealed that the small (nonsignificant) advantage of primed sperm when fertilization immediately follows insemination is reversed when eggs are fertilized by female‐stored sperm, weeks after insemination. By suggesting a plastic trade‐off between sperm velocity and viability, these results demonstrate that prolonged female sperm storage generates divergent selection pressures on ejaculate phenotype.

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The effects of male social environment on sperm phenotype and genome integrity

Cited by 22 publications

References 65 publications

Nongenetic paternal effects via seminal fluid

Nongenetic paternal effects via seminal fluid

Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish

Female sperm storage mediates post‐copulatory costs and benefits of ejaculate anticipatory plasticity in the guppy

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