Abstract
Loss of sex and recombination is generally assumed to impede the effectiveness of purifying selection and to result in the accumulation of slightly deleterious mutations. Empirical evidence for this has come from several studies investigating mutational load in a small number of individual genes. However, recent whole transcriptome based studies have yielded inconsistent results, hence questioning the validity of the assumption of mutational meltdown in asexual populations. Here, we study the effectiveness of purifying selection in eight asexual hexapod lineages and their sexual relatives, as present in the 1 K Insect Transcriptome Evolution (1KITE) project, covering eight hexapod groups. We analyse the accumulation of slightly deleterious nonsynonymous and synonymous point mutations in 99 single copy orthologue protein-coding loci shared among the investigated taxa. While accumulation rates of nonsynonymous mutations differed between genes and hexapod groups, we found no effect of reproductive mode on the effectiveness of purifying selection acting at nonsynonymous and synonymous sites. Although the setup of this study does not fully rule out nondetection of subtle effects, our data does not support the established consensus of asexual lineages undergoing ‘mutational meltdown’.
Highlights
The ubiquitous prevalence of sex among eukaryotes is surprising given that sexual reproduction involves manifold evolutionary costs as compared to obligate asexuality[1,2,3]
For Collembola and Phasmatodea, there was a significantly higher per-gene CDC in sexual as compared to asexual species indicating more effective selection on CUB in sexual species, whereas for Zygentoma and Sternorrhyncha there was a significantly lower per-gene CDC in sexual as compared to asexual species indicating more effective selection on CUB in asexual species. It has become established consensus among evolutionary biologists that sex and recombination increase the effectiveness of purifying selection, based on theoretical considerations and empirical evidence derived from a multiplicity of studies[12]
Our results do not match these studies: we find no evidence for accumulation of deleterious mutations in asexual hexapod species
Summary
The ubiquitous prevalence of sex among eukaryotes is surprising given that sexual reproduction involves manifold evolutionary costs as compared to obligate asexuality[1,2,3]. The rationale is that segregation, recombination and outcrossing enable the uncoupling of linked loci with different selection coefficients, such that selection can act on different loci independently[5] This accelerates adaptation and the purging of slightly deleterious mutations and facilitates the restoration of least loaded genotypes that are continuously lost by drift[5,6,7,8]. A multitude of studies have tested the prediction of impeded effectiveness of purifying selection (i.e. selective removal of deleterious mutations) in non-recombining genomic regions, such as mitochondria or (neo-) Y chromosomes as well as different lineages of asexual eukaryotes[10,11,12,13] Their results have led to the established consensus that slightly deleterious mutations accumulate in the absence of sex. We found extensive variation in dN/dS and CDC among genes and between hexapod groups, but no overall difference between reproductive modes
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