1 INTRODUCTION
Although sexual reproduction is the predominant mode of reproduction in
nearly all multicellular organisms, organisms reproducing only by
parthenogenesis (obligate parthenogens) are numerous. An important
ecological pattern is geographic parthenogenesis, a phenomenon where
parthenogens and their close sexual relatives occupy distinct geographic
areas. Parthenogens often have a biased distribution towards particular
environmental settings (e.g., high latitude, high altitude, and deserts)
when compared with close sexual relatives (Kearney, 2005). The loss of
sex (or success of parthenogens) in these particular environmental
settings has been an topic of interests in evolutionary biology,
shedding light on the cost and benefit of sex, adaptation to marginal
habitats, and the role of hybridization and polyploidy (e.g., Lynch,
1984; Bierzychudek, 1985; Kearney, 2005; Kawecki, 2008; Hörandl, 2009).
Although reports of geographic parthenogenesis from land and freshwater
are numerous, this occurrence has been rarely reported on from the sea.
Brown algae (Class Phaeophyceae, Stramenopiles) are one of few lineages
to have evolved complex multicellularity (Cock et al., 2010) and most of
them are exclusively marine. 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 (Luthringer et al.,
2014), and has been detected in sexual field populations at low
frequency (e.g., Oppliger et al., 2007; Klochkova et al., 2017; Hoshino
& Kogame, 2019). 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 Wynne, 1969; Müller, 1977; Peters, 1987; Deshmukhe &
Tatewaki, 1993; Hoshino et al., 2020a). However, there are only a few
reports in which these populations were compared with their close sexual
relatives and it remains largely unclear in what kind of environment
parthenogenesis is favored over sexual reproduction and how parthenogens
arise.
To the best of our knowledge, there are three cases in which brown algal
asexuals have been compared with close sexual relatives in detail. One
example is Fucus radicans , a species endemic to the brackish
water of the Baltic Sea (Bergström et al., 2005). Although
parthenogenesis is not known in this species, it has asexual populations
that are maintained by clonal reproduction using adventitious branches
(as dwarf morphotype of F. vesiculosus in Tatarenkov et al.,
2005). In this species, asexual populations tend to be distributed in
lower salinity areas than sexual populations (Ardehed et al., 2015). It
has been posited that low salinity restricts sexual reproduction due to
lysis of the egg cell or polyspermy
(Serrão et al., 1999), which could
favor a switch to asexual reproduction (Tatarenkov et al., 2005; Ardehed
et al., 2015). Although this is a convincing and interesting hypothesis
for the evolutionary process of asexual lineages, it cannot be applied
to asexuals living in saline environments where the majority of brown
algal asexuals occur. A second example is Mutimo cylindricus in
the Japanese Islands, where female-dominant parthenogenetic populations
are parapatric with sexual populations in the Tsugaru Strait (Figure 1;
the strait between Hokkaido and Honshu), the northern limit of this
species (as Cutleria cylindrica in Kitayama et al., 1992).
However, since sex ratio investigations over the entire distributional
area in Japan has not been conducted (Kitayama et al., 1992; Kogishi et
al., 2010), it is unclear if the parthenogens are geographically limited
to areas in the North.
The third known example is Scytosiphon lomentaria (Family
Scytosiphonaceae). This algae is distributed worldwide in warm and cold
temperate waters. In Japan, it has been reported from Hokkaido to Kyushu
(Figure 1; Hoshino et al, 2020c). It has a heteromorphic life history,
where generations of macroscopic dioicous isomorphic gametophytes
alternate with generations of microscopic discoid sporophytes (Nakamura
& Tatewaki, 1975). 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., 2014b). In culture
condition, both female and male gametes develop parthenogenetically
(Nakamura & Tatewaki, 1975). In these Japanese populations, in addition
to the sexual populations that included both female and male
gametophytes, parthenogenetic populations consisting of only females are
known (Hoshino et al., 2019). To date, parthenogenetic populations have
been found only in Hokkaido, and sexual populations have been reported
from southern Honshu (Hoshino et al., 2019). Females in the
parthenogenetic populations release gametes that are larger in size,
produce lesser sex pheromones, and their parthenogenetic development is
rapid, compared with females in the sexual populations (Hoshino et al.,
2019).
In the present study, we focused on S. lomentaria , aiming
to reveal what kind of
environments parthenogenesis is favored over sexual reproduction and how
parthenogens have arisen. To achieve this aim, we used samples from a
wide geographical range (33 localities across Japan, three localities
from Europe, and two localities from Argentina), we conducted (1) sex
ratio investigations, (2) phylogenetic and population genetic analyses
based on mitochondrial cox 1, nuclear cetn -int2, and
genome-wide single nucleotide polymorphism (SNP) markers, and (3)
crossing experiments and analyses of sex pheromone production.