A key role for sex chromosomes in the regulation of parthenogenesis in the brown alga Ectocarpus

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. Author summary Asexual reproduction is widespread among all major clades of eukaryotes. 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. Parthenogenesis has evolved independently in a wide variety of groups, but the genetic basis and the evolutionary forces driving transitions from sexual to parthenogenetic reproduction remain elusive. Here, we explore genetic, genomic and transcriptomic data from the brown alga Ectocarpus to uncover the genetic architecture of parthenogenesis. The brown algae are a group of complex multicellular organisms that have been evolving independently from animals and plants for more than a billion years, and they have recently emerged as important models to study the evolution of reproductive modes. 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. We identify several negative effects of parthenogenesis on male fitness and reveal evidence for trade-offs between sexual and asexual reproduction during the life cycle of Ectocarpus. Our results support the idea that parthenogenesis may be under both sex-specific selection and generation/ploidally-antagonistic selection, but the action of fluctuating selection on this trait may also contribute to the maintenance of polymorphisms in populations.