Directional postcopulatory sexual selection is associated with female sperm storage in Trinidadian guppies

Devigili, Alessandro; Nisio, Andrea Di; Grapputo, Alessandro; Pilastro, Andrea

doi:10.1111/evo.12989

Cited by 20 publications

(28 citation statements)

References 114 publications

(248 reference statements)

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“…We therefore gave priority to maintaining the effective population size in the same range as that used in the previous generations and in other studies (e.g., Ahuja and Singh 2008;Hine et al 2011). We interrupted the experimental evolution experiment after three generations because, due to the variance in the female maturation date (from 70 to 88 days, Reznick and Endler 1982) and the time between mating to first viable parturition (from 21 to 60 days, Devigili et al 2016), it became difficult to distinguish between different generations, which ultimately would have led to generations overlapping within replicates.…”

Section: Experimental Evolution Protocolmentioning

confidence: 99%

Stabilizing selection on sperm number revealed by artificial selection and experimental evolution

2018

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Sperm competition is taxonomically widespread in animals and is usually associated with large sperm production, being the number of sperm in the competing pool the prime predictor of fertilization success. Despite the strong postcopulatory selection acting directionally on sperm production, its genetic variance is often very high. This can be explained by trade-offs between sperm production and traits associated with mate acquisition or survival, that may contribute to generate an overall stabilizing selection. To investigate this hypothesis, we first artificially selected male guppies (Poecilia reticulata) for high and low sperm production for three generations, while simultaneously removing sexual selection. Then, we interrupted artificial selection and restored sexual selection. Sperm production responded to divergent selection in one generation, and when we restored sexual selection, both high and low lines converged back to the mean sperm production of the original population within two generations, indicating that sperm number is subject to strong stabilizing total sexual selection (i.e., selection acting simultaneously on all traits associated with reproductive success). We discuss the possible mechanisms responsible for the maintenance of high genetic variability in sperm production despite strong selection acting on it.

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Section: Experimental Evolution Protocolmentioning

confidence: 99%

Stabilizing selection on sperm number revealed by artificial selection and experimental evolution

2018

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“…Paternity was assigned using CERVUS v 3.0 (http://www.fieldgenetics.com/pages/home.jsp; Kalinowski, Taper, & Marshall, 2007; Marshall, Slate, Kruuk, & Pemberton, 1998). The data set included 561 offspring (from 36 females, 16 of which produced only the first brood and 20 of which produced two broods) of which 478 (i.e., 85%) were all assigned to one of the two competing FP‐FA males with >95% confidence probability (see Devigili et al., 2016, for more details; Devigili, Evans, Di Nisio, & Pilastro, 2015). The average paternity assignment success for each female was 88%.…”

Section: Methodsmentioning

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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“…However, despite evidence from guppies for inbreeding depression in ejaculate quality (Gasparini et al, 2013;Zajitschek & Brooks, 2010) and competitive fertilization success (Zajitschek et al, 2009), a recent study reported no significant association between heterozygosity and sperm competition success in a laboratory population of guppies (Devigili, Di Nisio, Grapputo, & Pilastro, 2016).…”

Section: Natural Populations Of Trinidadian Guppies (Poecilia Reticulmentioning

confidence: 95%

“…There is also evidence from a recent study of a single Venezuelan population of guppies revealing a highly significant association between microsatellite heterozygosity and orange coloration area (Herdegen, Dudka, & Radwan, ). However, despite evidence from guppies for inbreeding depression in ejaculate quality (Gasparini et al., ; Zajitschek & Brooks, ) and competitive fertilization success (Zajitschek et al., ), a recent study reported no significant association between heterozygosity and sperm competition success in a laboratory population of guppies (Devigili, Di Nisio, Grapputo, & Pilastro, ).…”

Section: Introductionmentioning

confidence: 97%

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

et al. 2017

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Heterozygosity-fitness correlations (HFCs) have been examined in a wide diversity of contexts, and the results are often used to infer the role of inbreeding in natural populations. Although population demography, reflected in population-level genetic parameters such as allelic diversity or identity disequilibrium, is expected to play a role in the emergence and detectability of HFCs, direct comparisons of variation in HFCs across many populations of the same species, with different genetic histories, are rare. Here, we examined the relationship between individual microsatellite heterozygosity and a range of sexually selected traits in 660 male guppies from 22 natural populations in Trinidad. Similar to previous studies, observed HFCs were weak overall. However, variation in HFCs among populations was high for some traits (although these variances were not statistically different from zero). Population-level genetic parameters, specifically genetic diversity levels (number of alleles, observed/expected heterozygosity) and measures of identity disequilibrium (g2 and heterozygosity-heterozygosity correlations), were not associated with variation in population-level HFCs. This latter result indicates that these metrics do not necessarily provide a reliable predictor of HFC effect sizes across populations. Importantly, diversity and identity disequilibrium statistics were not correlated, providing empirical evidence that these metrics capture different essential characteristics of populations. A complex genetic architecture likely underpins multiple fitness traits, including those associated with male fitness, which may have reduced our ability to detect HFCs in guppy populations. Further advances in this field would benefit from additional research to determine the demographic contexts in which HFCs are most likely to occur.

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Directional postcopulatory sexual selection is associated with female sperm storage in Trinidadian guppies

Cited by 20 publications

References 114 publications

Stabilizing selection on sperm number revealed by artificial selection and experimental evolution

Stabilizing selection on sperm number revealed by artificial selection and experimental evolution

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

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

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