Abstract
Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of these shifts remain largely elusive. Here, we used classic quantitative trait analysis, combined with genomic and transcriptomic information to dissect the genetic basis of asexual, parthenogenetic reproduction in the brown alga Ectocarpus. We found that parthenogenesis is controlled by the sex locus, together with two additional autosomal loci, highlighting the key role of the sex chromosome as a major regulator of asexual reproduction. We identify several negative effects of parthenogenesis on male fitness, and different fitness effects of parthenogenetic capacity depending on the life cycle generation. Although allele frequencies in natural populations are currently unknown, we discuss the possibility that parthenogenesis may be under both sex-specific selection and generation/ploidally-antagonistic selection, and/or that the action of fluctuating selection on this trait may contribute to the maintenance of polymorphisms in populations. Importantly, our data provide the first empirical illustration, to our knowledge, of a trade-off between the haploid and diploid stages of the life cycle, where distinct parthenogenesis alleles have opposing effects on sexual and asexual reproduction and may help maintain genetic variation. These types of fitness trade-offs have profound evolutionary implications in natural populations and may structure life history evolution in organisms with haploid-diploid life cycles.
Highlights
Sexual reproduction, involving meiosis and gamete fusion, is almost ubiquitous across eukaryotes, transitions to asexual reproduction have arisen remarkably frequently [1]
Parthenogenesis represents a specific mode of asexual reproduction, secondarily derived from sexual reproduction, and refers to the development of a multicellular organism from an unfertilised gamete
We show that parthenogenesis is a complex genetic trait under the control of the sex locus, together with two additional autosomal quantitative trait loci, highlighting the critical role for the sex chromosomes in the control of asexual reproduction in this organism
Summary
Sexual reproduction, involving meiosis and gamete fusion, is almost ubiquitous across eukaryotes, transitions to asexual reproduction have arisen remarkably frequently [1]. These asexual reproductive mechanisms include parthenogenesis, which involves the development of an embryo from an unfertilized gamete [1]. The genetic basis of parthenogenesis remains largely elusive in both plants and animals, the factors triggering the transition to asexual reproduction have been most intensively studied in plants, motivated by the potential use of asexual multiplication in the production of agricultural crops (e.g.[2,3]). Parthenogenesis is a component of apomixis, which is the asexual formation of seeds, resulting in progeny that are genetically identical to the mother plant. Apomeiosis is followed by parthenogenesis, which leads to the development of the diploid egg cell into an embryo, in the absence of fertilization (reviewed in [4])
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