4.3 The origin of parthenogens
Molecular analyses demonstrated that parthenogens have evolved at least
twice in S. lomentaria . Parthenogens from the Sea of Japan coast
and those from the Pacific coast probably have independent origins.
Parthenogens from the Sea of Japan coast (p1, p2, and p4) likely have
evolved from the sexuals of the west coast of Hokkaido (p3, p5, and p6)
which are the closest sexual relatives. Although p33 is in the Pacific
coast, it was genetically close to parthenogens from the Sea of Japan.
It may suggest that parthenogens from the Sea of Japan coast have spread
to the Pacific coast along ocean currents (Figure. 1). Parthenogens from
the Pacific coast (p26, p28, p29, and p32) were genetically the closest
to the sexuals of the Pacific coast (p19–p22 and p25), suggesting that
the parthenogens have evolved around the northern limit of sexuals in
the Pacific coast. In the NeighborNet, parthenogens of p24 and p27 and
those around the Tsugaru Strait (p30–p32) appeared to be distinct
lineages from those of the Sea of Japan (p1, p2, and p4) and the Pacific
coast (p26, p28, p29, and p32). However, judging from the results of
STRUCTURE analyses and PCA, they probably originated from hybridization
between sexuals from the Sea of Japan coast and existing parthenogens
from the Pacific coast (i.e., contagious origin; Simon et al., 2003).
Polyploidy of parthenogens of p24 and p27 may indicate that meiosis was
disturbed for some reason after the hybridization. Although a backcross
with their parental sexuals has been considered a taboo for the
maintenance of parthenogens (Lynch, 1984), it might have occurred
multiple times in S. lomentaria and provided genetic diversity in
parthenogens. Parthenogens of organisms having a haploid generation likeS. lomentaria are expected to be more susceptible to the
accumulation of deleterious mutations compared with parthenogens having
diploid or higher ploidy. In S. lomentaria parthenogens,
backcrosses with sexual relatives may have the benefits of eliminating
accumulated mutations and acquiring a new genome. However, considering
that there are sexual populations that probably originated from
hybridization between parthenogens and sexuals (p4, p5, p25; Figure 5),
some parthenogens may have been assimilated into sexuals through
hybridization. It may suggest that parthenogens also have a risk of
extinction through hybridization with their parental sexuals, as Lynch
(1984) pointed out.
Although the origins of parthenogens are not always known,
inter-specific hybridization and polyploidy are considered as major
triggers for parthenogenesis in animals and land plants
(Simon et al., 2003; Kearney,
2005; Hörandl, 2009). But it is probably not the case for S.
lomentaria . The parthenogenetic populations did not show evidence for
inter-specific hybridization, such as mitochondrial introgression. Some
parthenogenetic individuals seemed to be polyploid; however,cetn -int2 analysis showed that these polyploid samples from p24
and p27 originated from intra-specific crossing, not inter-specific
hybridization as we mentioned above.
The most plausible explanation for the origin of S. lomentariaparthenogens might be the spontaneous origin, that is, spontaneous loss
of sexuality or acquisition of asexuality through mutation (Simon et
al., 2003). In S. lomentaria , parthenogenesis of unfused gametes
is common in culture condition, even in individuals from sexual
populations (Hoshino et al., 2019). Thus, we expect that if sexual
reproduction is somehow disturbed (e.g., due to environmental factors or
loss of sexual traits), parthenogenetic ability will be under strong
selection and individuals with high parthenogenetic ability, that is
high enough to maintain obligate parthenogenetic life cycle, will be
easily selected. Although S. 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 et
al., 2019; Hoshino & Kogame, 2019). Females are likely to have more
potential than males to evolve into parthenogens in this species.
We have shown parallel suppression/loss of sex pheromone production in
parthenogens from the Sea of Japan coast and from the Pacific coast
(Hoshino et al., 2019; this study). Sex pheromone production can be
considered an essential trait for effective sexual reproduction, and the
spontaneous loss of such traits can trigger the evolution of
parthenogens. So, suppression/loss of sex pheromone production can be
considered the direct origin of the parthenogens. Another possible
explanation is that sex pheromone production was suppressed after the
evolution of parthenogens due to regressive evolution. In asexual life
cycles, sex pheromone production is useless and can be considered a
neutral or maladaptive trait depending on the amount of energy cost
required for their expression as we pointed out previously (Hoshino et
al., 2019). It has been suggested that a formerly adaptive trait can be
reduced, when that trait is neutral or maladaptive in the new selective
environment (Lynch, 1984; Lahti et al., 2009; van der Kooi & Schwander,
2014). In animal parthenogens, the decay of female sexual traits has
been widely reported (van der Kooi & Schwander, 2014). At present, it
is unclear whether the suppression/loss of sex pheromone production inS. lomentaria occurred before or after the evolution of
parthenogens.