Selection Is No More Efficient in Haploid than in Diploid Life Stages of an Angiosperm and a Moss

Szövényi, Péter; Ricca, Mariana; Hock, Zsófia; Shaw, Jonathan; Shimizu, Kentaro; Wagner, Andreas

doi:10.1093/molbev/mst095

Cited by 44 publications

(70 citation statements)

References 64 publications

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“…Thus, inbreeding affects life-history traits of both females and males, and these effects depend on the extent of unique female expression of genes affecting the traits (see also the concept of narrow expression breadth and its effect on purging; Szövenyi et al, 2013). Hence, our results support the hypothesis that in haplodiploids the degree of female genetic control determines the amount of genetic variation for a life-history trait due to deleterious recessive alleles.…”

Section: Resultssupporting

confidence: 75%

Inbreeding depression and purging in a haplodiploid: gender-related effects

2014

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Compared with diploid species, haplodiploids suffer less inbreeding depression because male haploidy imposes purifying selection on recessive deleterious alleles. However, alleles of genes only expressed in the diploid females are protected in heterozygous individuals. This leads to the prediction that haplodiploids suffer more from inbreeding effects on life-history traits controlled by genes with female-limited expression. To test this, we used a wild population of the haplodiploid mite Tetranychus urticae. First, negative effects of inbreeding were investigated by comparing maturation rate, juvenile survival, oviposition rate and longevity between lines created by three generations of either outbreeding or mother-son inbreeding. Second, purging through inbreeding was investigated by comparing the intensity of inbreeding depression between outbred families with known inbreeding/outbreeding mating histories. Negative effects of inbreeding and evidence for purging were found for the female trait oviposition rate, but not for juvenile survival and longevity. Both male and female maturation rate were negatively affected by inbreeding, most likely due to maternal effects because inbred offspring of outbred mothers was not affected. These results support the hypothesis that, in haplodiploids inbreeding effects and genetic variation due to deleterious recessive alleles may depend on gender.

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Section: Resultssupporting

confidence: 75%

Inbreeding depression and purging in a haplodiploid: gender-related effects

2014

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“…If, however, it is also true in general, then there are important consequences on the dynamics of adaptation (Sellis et al 2011). We thus believe that a comprehensive comparison of adaptation in haploids and diploids is necessary and must involve multiple aspects of adaptation, such as the dynamics, rate of evolution, and size of mutation effects, and must also address the changes of ploidy in life cycles (Orr and Otto 1994;Gerstein and Otto 2009;Gerstein et al 2012;Szövényi et al 2013;Selmecki et al 2015). sporulate 4.2L…”

Section: Limitations and Future Directionsmentioning

confidence: 99%

Heterozygote Advantage Is a Common Outcome of Adaptation inSaccharomyces cerevisiae

et al. 2016

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Adaptation in diploids is predicted to proceed via mutations that are at least partially dominant in fitness. Recently, we argued that many adaptive mutations might also be commonly overdominant in fitness. Natural (directional) selection acting on overdominant mutations should drive them into the population but then, instead of bringing them to fixation, should maintain them as balanced polymorphisms via heterozygote advantage. If true, this would make adaptive evolution in sexual diploids differ drastically from that of haploids. The validity of this prediction has not yet been tested experimentally. Here, we performed four replicate evolutionary experiments with diploid yeast populations (Saccharomyces cerevisiae) growing in glucose-limited continuous cultures. We sequenced 24 evolved clones and identified initial adaptive mutations in all four chemostats. The first adaptive mutations in all four chemostats were three copy number variations, all of which proved to be overdominant in fitness. The fact that fitness overdominant mutations were always the first step in independent adaptive walks supports the prediction that heterozygote advantage can arise as a common outcome of directional selection in diploids and demonstrates that overdominance of de novo adaptive mutations in diploids is not rare.KEYWORDS heterozygote advantage; experimental evolution; adaptation; diploid T HE most immediate difference between diploids and haploids is that diploids have twice as many gene copies and thus roughly twice as many expected mutations per individual per generation, assuming the same mutation rate per nucleotide. If adaptation is limited by the waiting time for new adaptive mutations, this suggests that diploids might enjoy an adaptive advantage over haploids; indeed, it has been argued that the rate of adaptive evolution in diploids might be double that in haploids (Paquin and Adams 1983;Anderson et al. 2004) [although see Zeyl et al. (2003) and Gerstein et al. (2011)].Diploids, however, might also suffer an adaptive disadvantage. New mutations in diploids are heterozygous, and their effect is thus "diluted" or even completely masked by the presence of the ancestral allele. Unless mutations are fully dominant in fitness, this reduces the probability of fixation of new beneficial mutations and increases the expected frequency that can be reached by deleterious mutations. This fitness effect "dilution" also slows down fixation of adaptive alleles in diploids by roughly twofold when adaptive mutations are codominant in fitness, and by more than that when adaptive mutations are either recessive (they spread in the population slowly) or fully dominant (they suffer a slowdown at high frequencies). This suggests that haploids should gain an advantage in adapting to new environments when the rate of spread of adaptive mutations is the limiting step in adaptation.These considerations have underpinned a large body of theory (Otto and Gerstein 2008) and generated some specific predictions. One of these is known as Hal...

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“…Although they may therefore experience some amount of selfing (Eppley et al 2007; Szövényi et al 2009), we refer to them as outcrossers to distinguish them from the more extreme selfers P. patens and F. hygrometrica. Importantly, the divergence times between the selfer and outcrosser species pairs are similar (McDaniel et al 2010; Shaw et al 2010; Liu et al 2012; Szövényi et al 2013). …”

Section: Methodsmentioning

confidence: 99%

“…To estimate the incidence of such mutations, we used high-throughput sequencing to generate two genome-wide transcriptome data sets for this study ( S. subsecundum and S. cribrosum ) and employed another such data set from our previous work ( F. hygromerica ) (Szövényi et al 2013). Briefly, for F. hygrometrica we had collected samples of three haploid and three diploid developmental stages, extracted RNA, and performed sequencing on an Illumina GAIIx machine that generated 173,542,944 raw reads.…”

Section: Methodsmentioning

confidence: 99%

“…If we assume that only diploid-specific genes are subject to purging, then the genome-wide effect of intragametophytic selfing on the accumulation of deleterious mutations should be minor (Szövényi et al 2011). This is because only very few genes are diploid-specific (2–3%; Szövényi et al 2011, 2013) and because genes also expressed in the haploid phase may not be affected by purging due to effective haploid selection (Klekowski 1973, 1982; Lloyd 1974; McCauley et al 1985; Taylor et al 2007; Eppley et al 2007; Billiard et al 2012). Alternatively, if genes expressed in both phases can also be affected by purging via homozygous exposure, intragametophytic selfing is expected to have a genome-wide effect because the majority of the genes is shared by the two phases (97%; Szövényi et al 2011, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Efficient Purging of Deleterious Mutations in Plants with Haploid Selfing

Szövényi

Devos

Weston

et al. 2014

Genome Biology and Evolution

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In diploid organisms, selfing reduces the efficiency of selection in removing deleterious mutations from a population. This need not be the case for all organisms. Some plants, for example, undergo an extreme form of selfing known as intragametophytic selfing, which immediately exposes all recessive deleterious mutations in a parental genome to selective purging. Here, we ask how effectively deleterious mutations are removed from such plants. Specifically, we study the extent to which deleterious mutations accumulate in a predominantly selfing and a predominantly outcrossing pair of moss species, using genome-wide transcriptome data. We find that the selfing species purge significantly more nonsynonymous mutations, as well as a greater proportion of radical amino acid changes which alter physicochemical properties of amino acids. Moreover, their purging of deleterious mutation is especially strong in conserved regions of protein-coding genes. Our observations show that selfing need not impede but can even accelerate the removal of deleterious mutations, and do so on a genome-wide scale.

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Selection Is No More Efficient in Haploid than in Diploid Life Stages of an Angiosperm and a Moss

Cited by 44 publications

References 64 publications

Inbreeding depression and purging in a haplodiploid: gender-related effects

Inbreeding depression and purging in a haplodiploid: gender-related effects

Heterozygote Advantage Is a Common Outcome of Adaptation inSaccharomyces cerevisiae

Efficient Purging of Deleterious Mutations in Plants with Haploid Selfing

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