4 DISCUSSION
Studies of population connectivity with mitochondrial markers provide
critical information on gene flow and genetic relationships between
neighboring populations (García, Vergara, & Gutiérrez, 2008; Turner,
McPhee, Campbell, & Winemiller, 2004). Many studies showed that
mitochondrial markers are highly effective for revealing marine fish
genetic diversity and population connectivity (T. Gao et al., 2019;
Lavergne et al., 2014; Machado et al., 2020). In this study onE. cardinalis , mtDNA
sequence analysis of specimens from Beibu Gulf revealed no significant
genetic
differentiation among sampling sites, with low ΦSTvalues indicating genetic homogeneity.
In contrast to freshwater species, marine fish are usually expected to
show low genetic differentiation across their distribution. This is
mainly attributed to genetic exchange being maintained by adult mobility
throughout Beibu Gulf during reproduction, and through the passive
dispersal of eggs and larvae due to the lack of noticeable physical
barriers in “open” oceans (Grant & Bowen, 1998; Hellberg, 2009;
Machado et al., 2020). The dominant widespread haplotype H1 was found in
all 11 sampling sites, which also indicated high dispersal potential of
planktonic egg, larval, or adult stages of E. cardinalis in Beibu
Gulf.
Previous studies suggested that E. cardinalis breed once a year
in Beibu Gulf (Z. Z. Chen & Qiu, 2003; Hou, Feng, Lu, & Zhu, 2008).Evynnis cardinalis gonads begin to develop in November and
spawning occurs from December to February. The population is
concentrated in the northern Beibu Gulf during spawning. In the early
spring, spawned fish mainly occur in the northeast of the gulf, and
juveniles concentrate in shallow nearshore of this area in the late
spring. Then, juveniles gradually migrate southwest and widely disperse
in deep waters of Beibu Gulf in summer or early autumn (K. Zhang et al.,
2020).
In addition, the dispersal pattern of E. cardinalis was also
impacted by circulation in Beibu Gulf. In spring, the density gradient
and monsoon wind drive the ocean current from northeast to southwest in
the gulf. The surface current velocity reaches 30 cm/s, and the current
in the middle layer is approximately 5–10 cm/s (J. Gao, Wu, & Ya,
2017). The direction of the spring currents roughly coincides with the
migration of E. cardinalis . Therefore, the seasonal migration and
ocean current may be responsible for gene exchange among different
locations, and therefore why E. cardinalis shows low levels of
genetic differentiation in Beibu Gulf. If we refer to the biological
description of a stock as given by Ihssen et al. (1981), “a stock is an
intraspecific group of randomly mating individuals with temporal and
spatial integrity,” then the lack of distinct spatial boundaries and
genetic substructure (low ΦST values) revealed by
genetic analyses indicated that E. cardinalis in Beibu Gulf
belong to a single stock.
The presence of a single stock in Beibu Gulf indicates that geographical
isolation might block gene exchange between the Beibu Gulf stock and the
other two E. cardinalis stocks, the Taiwan Strait and South China
Sea stocks. In Beibu Gulf, the circulation, Hainan Island, and Leizhou
Peninsula could act as barriers that impede free dispersal of E.
cardinalis into this gulf from other areas of the South China Sea (J.
Gao et al., 2017). The findings from our study and similar
investigations conducted elsewhere demonstrated that marine fish that
inhabit coastal waters usually constitute a single panmictic stock. For
example, Rodrigues et al. (2008) revealed that Cynoscion acoupafrom northern Brazil represents a single stock, even though it occupies
at least 1260 km of coastline. T. Gao et al. (2019) reported a high
level of genetic homogeneity in the Pholis fangi population
around Bohai Sea and Yellow Sea, and suggested it should be considered
as a single panmictic stock. Hoolihan, Anandh, and van Herwerden (2006)
also reported a homogeneous distribution of Spanish mackerel
(Scomberomorus commerson ) throughout the Arabian Gulf, Gulf of
Oman, and Arabian Sea on the basis of mtDNA analyses.
In addition, mtDNA sequence regions are particularly appropriate to
infer historical processes that might be responsible for the
contemporary geographic distribution of marine species because they are
more prone to genetic drift than nuclear markers and have a smaller
effective population size (Avise, 1994; Slatkin & Hudson, 1991).
In our study, the haplotype
network of E. cardinalis from Beibu Gulf exhibited a star-like
and unstructured pattern with a predominance of scattered. The dominant
haplotype (carried by 45% of the specimens) was in the central position
of the haplotype network and surrounded by many haplotypes that diverged
from the dominant haplotype by only few mutations. Most surrounding
haplotypes were unique to each sampling site and showed few differences
between them (Fig. 2). Similar star-like haplotype networks have been
observed for other species in different coastal areas: Terapon
jarbua , which consists of a panmictic stock from the Socotra
Archipelago to the Hadhramout Coast along the wider Gulf of Aden
(Lavergne et al., 2014); and Pogonias courbina , which did not
display distinct structure along the coast of the southwestern Atlantic
Ocean (Machado et al., 2020).
A star-like haplotype network pattern, high haplotype diversity, and low
nucleotide diversity are often considered consequences of recent
population expansion linked to the Pleistocene environmental changes
(Craig, Eble, Bowen, & Robertson, 2007; Liu et al., 2011; Pereira,
Márquez, Marin, & Marin, 2009). The recent demographic expansion ofE. cardinalis from Beibu Gulf is also supported by the unimodal
mismatch distribution and significantly negative Tajima’s D and Fu’s Fs
values. The population expansion of E. cardinalis in Beibu Gulf,
which was directly estimated from the mismatch distribution, started
62–21 ka before present, which was during the late Pleistocene. BSP
analysis indicated steady population expansion that started around 30
ka. Both two methods of estimated period of
population expansion are
consistent with the environment changes of the northern South China Sea
in the Pleistocene.
Evynnis cardinalis is primarily distributed from 30–60 m depth,
and spawns in coastal habitats and shallow shorelines. Therefore, theE. cardinalis distribution is closely correlated with fluctuating
sea levels. When sea levels fell 120 m below the present level during
the last glacial maximum of the Pleistocene, the northern South China
Sea included Beibu Gulf, which was part of the South China continent,
Hainan Island and Taiwan Island were connected to mainland China, and
the entire South China Sea was separated from the Indian Ocean to form a
semi-closed basin (Voris, 2000; P. Wang & Sun, 1994). Similar to other
terrestrial species, E. cardinalis may have moved and survived in
a potential glacial refuge during this period, such as the semi-closed
South China Sea (Hewitt, 1999). In the late Pleistocene, the sea level
was still 30 m below the present level, but the glaciation began to
disappear and the sea water gradually poured into Beibu Gulf via the
Qiongzhou Strait (Lu, Huang, Li, & Zhang, 2003). An initial population
of E. cardinalis may have immigrated to Beibu Gulf from
neighboring areas after it was filled with sea water and sufficiently
deep. This initial panmictic stock quickly colonized the empty novel
environment under the founder and priority effects, and experienced
rapid population expansion when favorable conditions occurred (Boileau,
Hebert, & Schwartz, 1992; Shulman et al., 1983).