Temperature-driven mitochondrial lineage splitting
Phylogeographic patterns of marine organisms in the NWP are shaped by
the interplay of historical and/or contemporary oceanography, and
present-day gene flow, which is often correlated with species-specific
life-history features such as larval traits (Cheang et al., 2012). The
timing of lineage splitting event between the two M. virgatalineages is estimated to be 5.49-1.61 Mya. Although there is substantial
deviation between estimates using the lowest and highest calibration
bounds of the molecular clock, the estimated divergence time coincides
with the glacial periods from the Pliocene to Pleistocene epochs. Sea
level fluctuation during this time affected population fragmentation and
demographic changes for many coastal species, resulting in population
structuring and/or lineage splitting in the NWP (Shen et al., 2011; Ludt
& Rocha, 2014).Cyclic alternations of glacial-interglacial periods
dramatically affected the seafloor topography and sea level dropped up
to 120 m below its present level during the glacial periods (i.e., early
Pleiostocene), resulting in historical isolation in the NW Pacific
marginal seas: Pleiostocene isolation of the ES/JS, ECS, and SCS (Wang,
1999; Voris, 2000). The ES/JS was semi-enclosed and prevailed by cold
surface water flows from the northern sea during the Northern Hemisphere
glaciation and mid-Pleiostocene transition (Tada, 1994; Kitamura et al.,
2001; Matsuzaki, Itaki, Tada, & Kamikuri, 2018). Meanwhile, the SCS was
separated from the ECS (Ota, 1998; see Fig. 7 for details) by a large
land bridge extending between eastern China and Taiwan Island (Kimura,
2000). Peng et al. (2019) found that there is a post-LGM expansion ofM. virgatus in Zhejiang, China (belonging to the southern lineage
in the present study), based on population genetic analysis of mtDNAcox1 and 16S rDNA sequences.
In addition to historical geography in the NWP, some environmental
factors (e.g., ocean current, surface water temperature and salinity)
might act in combination with stochastic processes such as local
selection and/or lineage sorting through time in shaping contemporary
population structure (Palumbi, 1994; Miglietta, Faucci, & Santini,
2011). In our results, the geographic distribution of the two
mitochondrial lineages agrees with two biogeographic regions with
different surface water temperature zones: the northern lineage occupies
the North Pacific Temperate Biotic Region which is affected by the
cold-water Liman Current flowing southward from the Sea of Okhotsk into
in the East Sea (the Sea of Japan) and the Oyashio Current (also known
as the Kurile Current) that flows south and meets the Kuroshio Current
off the eastern shore of Japan. In contrast, the southern lineages are
occupied by Chinese populations, Taiwan population and the southern
Japan populations, all belonging to the Indo-West Pacific warm-water
Biotic Region which is affected by the warm, northeasterly flowing
Kuroshio Current. It is interesting to note that some Japanese
populations where the two lineages co-occur (JSH, JSS, JKS, JOI, JKG,
JNG; Table 1 and Fig. 1) agree well with the region where two currents
with different surface water temperatures meet: JOI (16), JKG (17), and
JNG (18) are found on the western side of Japanese archipelago where the
cold-water carrying Liman Current (LC) and the warm-water carrying
Tsushima Warm Current (TSWC) meet in the North Pacific Temperate Biotic
Region, whereas JSH (8), JSS (9), and JKS (11) are found in southeastern
side of Japan where the Kuroshio Current (KC) mixes with the
southeasterly flowing, cold-water carrying Oyashio Current (OC) in the
Indo-West Pacific warm-water Biotic Region.
Present-day oceanic currents are among the most influential factors that
contribute to continuous gene flow over a wide geographic range in many
marine invertebrates, including molluscan species (Dong et al., 2012;
Guo et al., 2015; Li et al., 2017). M. virgata has a planktonic
larval stage for 4 days, allowing them to disperse considerable
distances via northeasterly flowing ocean currents (Sasaki, 1984). The
present-day geographic distribution of the northern and southern
lineages is assumed to be due to current-driven long-distance dispersal
of planktonic larva from the northern and southern glacial refugia. Deep
lineage splitting and geographic distribution of the two mitochondrial
lineages uncovered in this study suggest that along with ocean currents,
surface water temperature preference and/or differential selection
between the respective ancestral populations of the southern and
northern lineages have shaped contemporary phylogeographic patterns: The
ancestral population of the northern lineage would have been under
selection for adaptation to colder water, while the southern lineage
might have adapted to a warmer environment. This thermal adaptation
likely restricted gene flow between the two regional populations by
reducing migrant fitness, resulting in lineage splitting along a
temperature gradient (Teske, Von der Heyden, McQuaid, & Barker, 2011;
Teske et al., 2019). Such a vicariant lineage splitting following
long-term adaptation to different temperature zones has been reported in
some other marine species including mantis shrimp (Cheng & Sha, 2017),
mitten crab (Xu et al., 2009), barnacles (Tsang et al. 2012), and
flathead mullet (Shen et al., 2011). We cautiously suggest that cryptic
mitochondrial lineage splitting in M. virgata might be the result
of an adaptive response (i.e., a balancing selection) to different
environments, most likely different surface water temperature zones. An
extensive genetic survey of nuclear genes, along with in-depth analysis
of balancing selection from mitochondrial genome sequences, would be
needed to clarify how these two mitochondrial lineages have adapted in
response to thermal differences in the NWP.