The Evolutionary Consequences of Selection at the Haploid Gametic Stage

Immler, Simone; Otto, Sarah P.

doi:10.1086/698483

Cited by 66 publications

(73 citation statements)

References 103 publications

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“…Nevertheless, recent studies have demonstrated that sperm competition, even within a single 386 ejaculate, can alter haploid allele frequencies and increase offspring fitness [67,68]. Expression in the gamete is 387 not required for haploid selection if the fitness of a gamete depends on its ability to condense DNA [69]. 388 Furthermore, expression during gamete production often underlies systems of meiotic drive [70][71][72], which may be 389 a common form of haploid selection in animals [73].…”

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confidence: 99%

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Scott

Osmond

Otto

2018

Preprint

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Sex determination is remarkably dynamic; many taxa display shifts in the location of sex-determining loci or the evolution of entirely new sex-determining systems. Predominant theories for why we observe such transitions generally conclude that novel sex-determining systems are favoured by selection if they equalise the sex ratio or increase linkage with a locus that experiences different selection in males vs. females. We use population genetic models to extend these theories in two ways: (1) We consider the dynamics of loci very tightly linked to the ancestral sex-determining loci, e.g., within the non-recombining region of the ancestral sex chromosomes. Variation at such loci can favour the spread of new sex-determining systems in which the heterogametic sex changes (XY to ZW or ZW to XY) and the new sex-determining region is less closely linked (or even unlinked) to the locus under selection. (2) We consider selection upon haploid genotypes either during gametic competition (e.g., pollen competition) or meiosis (i.e., non-Mendelian segregation), which can cause the zygotic sex ratio to become biased. Haploid selection can drive transitions between sex-determining systems without requiring selection to act differently in diploid males vs. females. With haploid selection, we find that transitions between male and female heterogamety can evolve where linkage with the sex-determining locus is either strengthened or weakened. Furthermore, we find that sex-ratio biases may increase or decrease with the spread of new sex chromosomes, which implies that transitions between sex-determining systems cannot be simply predicted by selection to equalise the sex ratio. In fact, under many conditions, we find that transitions in sex determination are favoured equally strongly in cases where the sex ratio bias increases or decreases. Overall, our models predict that sex determination systems should be highly dynamic, particularly when haploid selection is present, consistent with the evolutionary lability of this trait in many taxa. Author summarySystems of sex determination are strikingly diverse and labile in many clades. This poses the question: what drives transitions between sex-determining systems? Here, we use models to derive conditions under which new sex-determining systems spread. Prevailing views suggest that new sex-determining systems are favoured when they equalize the sex ratio and/or when they are more closely linked to genes that experience differential selection in males and females. Our models include selection upon haploid genotypes (meiotic drive or gametic competition), which biases the sex-ratio and occurs differently in male and female gametes. Surprisingly, we find the two forces (selection to equalize the sex ratio and the benefits of hitchhiking alongside driven alleles that distort the sex ratio) will often be equally strong, and thus neither is sufficient to explain the spread of new sex-determining systems in every case. We also find that new sex-determining alleles can spread despite b...

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Section: /38mentioning

confidence: 99%

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Scott

Osmond

Otto

2018

Preprint

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“…; Barreau et al. ) and the scope for haploid gene expression and hence selection may be more important than assumed so far (Joseph and Kirkpatrick ; Immler ; Immler and Otto ). Even though the haploid phase is rather short in predominantly diploid organisms, selection occurring during the haploid gametic phase may have far reaching consequences for basic evolutionary processes including the rate of adaptation (Orr and Otto ), the genetic load (Charlesworth and Charlesworth ; Otto et al.…”

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confidence: 98%

“…), and genetic variation more generally (Immler et al. ; Immler and Otto ). However, empirical evidence for these effects is still scarce.…”

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confidence: 99%

“…Nevertheless, empirical evidence for gene expression in haploid spermatids is increasing (Fujimoto et al 1984;Barreau et al 2008) and the scope for haploid gene expression and hence selection may be more important than assumed so far (Joseph and Kirkpatrick 2004;Immler 2008;Immler and Otto 2018). Even though the haploid phase is rather short in predominantly diploid organisms, selection occurring during the haploid gametic phase may have far reaching consequences for basic evolutionary processes including the rate of adaptation (Orr and Otto 1994), the genetic load (Charlesworth and Charlesworth 1987;Otto et al 2015), and genetic variation more generally (Immler et al 2012;Immler and Otto 2018). However, empirical evidence for these effects is still scarce.…”

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Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring

et al. 2019

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Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within‐ejaculate sperm selection for sperm longevity increased the performance of the resulting offspring in several key life‐history traits in early life. Because increased early‐life reproductive performance often correlates with rapid ageing, it is possible that within‐ejaculate sperm selection increases early‐life fitness at the cost of accelerated senescence. Alternatively, within‐ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age‐specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio . We found that within‐ejaculate sperm selection for sperm longevity reduced age‐specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within‐ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early‐life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within‐ejaculate sperm selection also reduced the age‐specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within‐ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and may have important implications for assisted fertilization programs in livestock and humans.

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“…; Alavioon et al. ; Immler and Otto ). Direct observation of such early acting selection will be impossible in many taxa, while characterizing the genetic basis of viability is challenging given that fitness is highly polygenic, deleterious alleles are individually rare, and may have small effects (Visscher et al.…”

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Do slower movers have lower reproductive success and higher mutation load?

Walsh

McGuigan

2018

Evolution Letters

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Deleterious mutations occur frequently in eukaryotes, resulting in individuals carrying multiple alleles that decrease their fitness. At a population level, if unchecked, accumulation of this mutation load can ultimately lead to extinction. How selection counters the accumulation of mutation load, limiting declines in population fitness, is not well understood. Here, we use manipulative experiments in zebrafish (Danio rerio) to investigate the opportunities for selection on mutation load. Inducing high mutation load through mutagenesis, we applied one generation of within‐family selection on locomotor performance and characterized both the direct response to this selection and the indirect response of reproductive success. Offspring of slow swimming parents exhibited age‐dependent declines in swimming speed, whereas their cousins, with faster swimming parents, did not. This pattern mimics previously documented differences between high and low mutation load populations of zebrafish, suggesting that slow swimming siblings inherited (and transmitted) more mutations than their faster swimming siblings. Crosses among offspring of slow swimming fish had, on average, <75% of the reproductive success of crosses among offspring of fast swimming parents, or crosses of offspring of slow swimmers with offspring of fast swimmers. This evidence of mutationally correlated swimming speed and reproductive success reveals the potential for concordant selection on mutation load through different fitness components. There was no evidence that crosses within families (where parents potentially shared the same mutations inherited from their common ancestor) had lower reproductive success than crosses among families, suggesting that viability selection was not acting predominantly through lethal recessive homozygotes. Rather, patterns of reproductive success are suggestive of effects of mutation number per se on embryo viability. Overall, our results highlight the potential for early life mortality to remove deleterious mutations, and the need to account for this mortality when investigating the evolutionary dynamics of mutation load.

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The Evolutionary Consequences of Selection at the Haploid Gametic Stage

Cited by 66 publications

References 103 publications

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring

Do slower movers have lower reproductive success and higher mutation load?

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