title: Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera.
abstract: Sexual reproduction is nearly universal among eukaryotes. Theory predicts that the rarity of asexual eukaryotic species is in part caused by accumulation of deleterious mutations and heightened extinction risk associated with suppressed recombination and segregation in asexual species. We tested this prediction with a large data set of 62 transcriptomes from 29 species in the plant genus Oenothera, spanning ten independent transitions between sexual and a functionally asexual genetic system called permanent translocation heterozygosity. Illumina short-read sequencing and de novo transcript assembly yielded an average of 16.4 Mb of sequence per individual. Here, we show that functionally asexual species accumulate more deleterious mutations than sexual species using both population genomic and phylogenetic analysis. At an individual level, asexual species exhibited 1.8 × higher heterozygosity than sexual species. Within species, we detected a higher proportion of nonsynonymous polymorphism relative to synonymous variation within asexual compared with sexual species, indicating reduced efficacy of purifying selection. Asexual species also exhibited a greater proportion of transcripts with premature stop codons. The increased proportion of nonsynonymous mutations was also positively correlated with divergence time between sexual and asexual species, consistent with Muller's ratchet. Between species, we detected repeated increases in the ratio of nonsynonymous to synonymous divergence in asexual species compared with sexually reproducing sister taxa, indicating increased accumulation of deleterious mutations. These results confirm that an important advantage of sex is that it facilitates selection against deleterious alleles, which might help to explain the dearth of extant asexual species.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada Department of Biology, University of Toronto at Mississauga, Mississauga, ON, Canada jesse.hollister@utoronto.ca gane@ualberta.ca.
authors.forename: Jesse D
authors.initials: JD
authors.lastname: Hollister
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.
authors.forename: Stephan
authors.initials: S
authors.lastname: Greiner
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
authors.forename: Wei
authors.initials: W
authors.lastname: Wang
authors.affiliation: BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Yantian District, China.
authors.forename: Jun
authors.initials: J
authors.lastname: Wang
authors.affiliation: BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Yantian District, China.
authors.forename: Yong
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Yantian District, China Department of Biological Sciences and Department of Medicine, University of Alberta, Edmonton, AB, Canada jesse.hollister@utoronto.ca gane@ualberta.ca.
authors.forename: Gane Ka-Shu
authors.initials: GK
authors.lastname: Wong
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada jesse.hollister@utoronto.ca gane@ualberta.ca.
authors.forename: Stephen I
authors.initials: SI
authors.lastname: Wright
authors.affiliation: Department of Biology, University of Toronto at Mississauga, Mississauga, ON, Canada.
authors.forename: Marc T J
authors.initials: MT
authors.lastname: Johnson
mesh_terms: D018388:Codon, Terminator; D006579:Heterozygote; D009154:Mutation; D031664:Oenothera / Q000235:genetics* / Q000502:physiology; D010802:Phylogeny; D012100:Reproduction, Asexual / Q000235:genetics*; D059467:Transcriptome
chemical_list: D018388:Codon, Terminator
keywords: Muller’s ratchet; asexual reproduction; deleterious mutations; evolution of sex; purifying selection