Geographic parthenogenesis in the brown alga Scytosiphon lomentaria (Scytosiphonaceae): sexuals in warm waters and parthenogens in cold waters

Geographic parthenogenesis (GP), a phenomenon where parthenogens and their close sexual relatives inhabit distinct geographic areas, has been considered an interesting topic to understand the adaptation to marginal habitats and the role of hybridization in evolution. Reports of GP from land and freshwater are numerous, however, this occurrence has been rarely reported on from the sea. Brown algae are mostly marine and are thought to include numerous obligate parthenogens; still, little is known about the distribution, origin, and evolution of parthenogens in this group. Here we report a novel pattern of GP in the isogamous brown alga Scytosiphon lomentaria. Sex ratio investigation demonstrated that, in Japan, sexual populations grew in the coast along warm ocean currents, whereas female-dominant parthenogenetic populations grew mainly in the coast along a cold ocean current. In the two localities where sexual and parthenogenetic populations were parapatric, parthenogens grew in more wave-exposed areas than sexuals. Population genetic and phylogenetic analyses, including those based on genome-wide single nucleotide polymorphism data, suggested that: (1) parthenogens evolved at least twice in S. lomentaria, (2) parthenogens did not originate from inter-species hybridization, (3) new parthenogenetic lineages have arisen from hybridizations between parthenogens and sexuals, and (4) parthenogens have a wider distribution than sexuals. We also showed that the production of sex pheromones, which attract male gametes, has been independently suppressed/lost in two parthenogenetic lineages. This parallel suppression/loss of the sexual trait may represent the direct origin of parthenogens, or the regressive evolution of a useless trait under asexuality.