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

Abstract

Geographical parthenogenesis, a phenomenon where parthenogens and their close sexual relatives inhabit distinct geographical areas, has been considered an interesting topic in evolutionary biology. Reports of geographical parthenogenesis from land and freshwater are numerous, but this occurrence has been rarely reported 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 geographical parthenogenesis 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, indicated that parthenogens have initially evolved at least twice and subsequent hybridizations between the parthenogens and sexuals have generated multiple new parthenogenetic lineages. The origin of the initial parthenogens is not clear, except that it would not be interspecies hybridization. Interestingly, we found that the production of sex pheromones, which attract male gametes, has been independently lost in the initial two parthenogenetic lineages. This parallel loss of the sexual trait may represent the direct origin of parthenogens, or the regressive evolution of a useless trait under asexuality.

Parallel loss of sex in field populations of a brown alga sheds light on the mechanisms underlying the emergence of asexuality

“…We showed previously that gametes from S. lomentaria Amazon populations do not produce pheromone, although they still form zygotes with male gametes from sexual populations if gametes are incubated at high density in a small drop of seawater (Hoshino et al 2021). We tested whether gametes from S. promiscuus Amazon populations, likewise, were unable to produce the sexual pheromone.…”

“…In the brown alga S . lomentaria , however, phylogenetic analyses based on mitochondrial and nuclear markers have found no evidence for interspecific hybridization (Hoshino et al ., 2021). At least two scenarios are possible to explain the origin of the Amazon populations.…”

“…In the second scenario, males are less tolerant to a change in environmental conditions (e.g. water temperature, (Hoshino & Kogame, 2019; Hoshino et al ., 2021), so they become less frequent, which favours females that rapidly reproduce by parthenogenesis. As pheromone production is presumably costly, this trait would then be lost.…”

Uncovering the Male Presence in Parthenogenetic Marchalina hellenica (Hemiptera: Marchalinidae): Insights into Its mtDNA Divergence and Reproduction Strategy

“…Asexual reproduction would lead sexually reproduced natural enemies to become proficient at handling the defense mechanisms of a single clone, while their beneficiaries’ own capabilities would be continuously improved [ 85 ]. Furthermore, some species exhibit both sexual and parthenogenetic lineages on different hosts or in different geographical regions [ 24 , 74 , 86 ], with parthenogenetic populations often living within distinct ranges, such as marginal habitats, or at a higher latitude or altitude than sexual lineages [ 87 , 88 , 89 ]. Jensen et al [ 90 ] suggested that sexual populations, usually found at the central part of the range of the infestation, act as sources of populations choosing asexual reproduction, which are found in the marginal regions of infestations.…”

Role of transcription and translation during the early development of the brown algaEctocarpus

“…On the contrary, no parthenotes were identified among hundreds of Ectocarpus individuals from NW France and SW Italy (Couceiro et al ., 2015), indicating that if parthenogenesis does occur in wild populations, the fitness of parthenosporophytes may be lower than that of sexually obtained sporophytes in the same environment. However, fully parthenogenetic populations of the brown alga Scytosiphon lomentaria (Ectocarpales) have been described in Japan (Hoshino et al ., 2019), which potentially inhabit ecological niches unsuitable for sexual strains (Hoshino et al ., 2021).…”