Parthenogenesis is rare in the reproduction of a sexual field population of the isogamous brown alga Scytosiphon (Scytosiphonaceae, Ectocarpales)

Abstract

Parthenogenetic development of unfused gametes is commonly observed in laboratory cultures among various brown algal taxa. There is, however, little information on the contribution of parthenogenesis to the reproduction of field populations. In this study, we investigated whether parthenogenesis is present in a sexual population of the isogamous brown alga Scytosiphon with a 1:1 sex ratio. In culture, both female and male gametes showed higher mortality and slower development compared to zygotes. More than 90% of surviving partheno‐germlings formed parthenosporophytes irrespective of the culture conditions tested. Therefore, if parthenogenesis occurs in the field, most unfused gametes are expected to form parthenosporophytes. Contrary to this expectation, parthenosporophytes were rare in the field population. We collected 126 sporophytic thalli and isolated and cultured a unilocular sporangium from each of them. We confirmed that cultures of 120 unilocular sporangia produced both female and male gametophytes by the observation of zygotes or amplification of PCR‐based sex markers indicating that these sporangia originated from zygotic sporophytes. Only females were detected in cultures from two sporangia and only males from four sporangia suggesting that these sporangia originated from parthenosporophytes. In the Scytosiphon population, although parthenogenesis is observable in culture, our results demonstrate that the contribution of parthenogenesis to reproduction is small (≤4.8%) compared to sexual reproduction. Unfused gametes may not survive to form mature parthenosporophytes in significant numbers in the field partly due to their higher mortality and slower development compared from zygotes.

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

“…Histograms based on the haploid data set showed that pairs of individuals having genetic distances of less than 11 were rare in sexual populations (seven pairs out of a total of 7,021 pairs), but abundant in parthenogenetic populations (221 pairs out of a total of 4,278 pairs; Figure 4). A previous study showed that parthenogenesis rarely occurred in a sexual population of Scytosiphon shibazakiorum (as Scytosiphon species IIa; Hoshino & Kogame, 2019), a close relative of S . lomentaria .…”

“…lomentaria is isogamous and both female and male gametes have parthenogenetic ability, male parthenogens were not found. This is probably due to the more inferior parthenogenetic ability of male gametes than that of females (Hoshino & Kogame, 2019; Hoshino et al, 2019). Females are likely to have more potential than males to evolve into parthenogens in this species.…”

“…Its sexual reproduction is isogamous; female gametes settle on the substratum sooner than male gametes and secrete sex pheromones that attract male gametes (Fu et al, 2014). In culture conditions, both female and male gametes develop parthenogenetically, but male gametes show higher mortality during parthenogenetic development than female gametes; mortality of male gametes was 94%–97% and mortality of female gametes was 20–60% in the closely related species, Scytosiphon shibazakiorum (as Scytosiphon species IIa; Hoshino & Kogame, 2019). In S .…”

“…In brown algae, parthenogenesis, the development of a new individual from an unfertilized gamete, is a common phenomenon. Even in sexual lineages, parthenogenetic development of unfused gametes is common in laboratory cultures (Hori, 1993; Luthringer et al, 2014), and has been detected in sexual field populations at low frequency (e.g Hoshino & Kogame, 2019; Klochkova et al, 2017; Oppliger et al, 2007). There are numerous reports of brown algal populations which are speculated to have an obligate parthenogenetic life cycle (i.e., populations in which sexual reproduction cannot be observed; examples include Deshmukhe & Tatewaki, 1993; Hoshino et al, 2020; Müller, 1977; Peters, 1987; Wynne, 1969).…”

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

“…In the first scenario, a mutation leading to loss of pheromone production triggers the loss of sex (i.e., ‘spontaneous origin’, (Simon et al ., 2003). Because female gametes are capable of parthenogenesis, then the female-parthenogenetic population expands whereas males would decay because they cannot undergo efficient parthenogenesis (Hoshino & Kogame, 2019). In the second scenario, males are less tolerant to a change in environmental conditions (e.g.…”