Phylogeography of Bivalve Cyclina sinensis: Testing the Historical Glaciations and Changjiang River Outflow Hypotheses in Northwestern Pacific

Abstract

BackgroundThe marginal seas of northwestern Pacific are characterized by unique topography and intricate hydrology. Two hypotheses have been proposed to explain genetic patterns of marine species inhabiting the region: the historical glaciations hypothesis suggests population genetic divergence between sea basins, whereas the Changjiang River outflow hypothesis suggests genetic break in line with the Changjiang Estuary. Here the phylogeography of bivalve Cyclina sinensis was investigated to test the validity of these two hypotheses for intertidal species in three marginal seas—the East China Sea (ECS), the South China Sea (SCS), and the Japan Sea (JPS).Methodology/Principal FindingsFragments of two markers (mitochondrial COI and nuclear ITS-1) were sequenced for 335 individuals collected from 21 populations. Significant pairwise ΦST were observed between different marginal sea populations. Network analyses illustrated restricted distribution of haplogroups/sub-haplogroups to sea basins, with a narrow secondary contact zone between the ECS and SCS. Demographic expansion was inferred for ECS and SCS lineages using mismatch distributions, neutral tests, and extended Bayesian Skyline Plots. Based on a molecular clock method, the divergence times among COI lineages were estimated dating from the Pleistocene.ConclusionsThe phylogeographical break revealed for C. sinensis populations is congruent with the historical isolation of sea basins rather than the putative Changjiang River outflow barrier. The large land bridges extending between seas during glaciation allowed accumulation of mutations and subsequently gave rise to deep divergent lineages. The low-dispersal capacity of the clam and coastal oceanography may facilitate the maintenance of the historical patterns as barriers shift. Our study supports the historical glaciations hypothesis for interpreting present-day phylogeographical patterns of C. sinensis, and highlights the importance of historical glaciations for generating genetic structure of marine coastal species especially those with low-dispersal abilities in northwestern Pacific.

Genetic variation and population structure of the Pacific oyster Crassostrea gigas in the northwestern Pacific inferred from mitochondrial COI sequences

“…The level of genetic diversity of C. gigas was characterized by moderate haplotype diversity (4 of 12 populations had low values, including LZ, PL, ZS and SU) and low nucleotide diversity, which was partly consistent with the previous conclusions reported by Sekino et al [52]. In addition, the level of genetic variation for C. gigas was relatively lower than that of some co-distributed bivalves (Table 5), such as C. sinensis [13], Tegillarca granosa [14], Crassostrea ariakensis [53] and Atrina pectinate [21]. A different population history of these species was assumed to be responsible for the differences in genetic variations.…”

“…Therefore, marine organisms and their progenies might be divided into ECS, SCS, and JPS lineages after the rising of post-glacial sea levels. This observation has been reported in several organisms, such as C. haematocheilu [8] and C. sinensis [13]. Based on our sampling scope and the population genetic structure revealed, we infer that the unique lineage of C. gigas in the present study might belong to the ECS lineage.…”

“…The oceanographic processes (e.g., ocean currents) are related to genetic distribution in marine organisms over large spatial scales [6], which is particularly true for adult sedentary marine organisms [7]. There has been a growing number of studies highlighting the relationships among dispersal, gene flow, ocean currents and Pleistocene glacial-interglacial cycles in marine systems, including many species such as fishes [8,9], crustaceans [10,11], and mollusks [12][13][14][15].…”

“…The CDW has been considered to be an extrinsic barrier for genetic connectivity for some intertidal species, such as Cyclina sinensis [27] and Cellana toreuma [28], while the barrier effect of the Changjiang River outflow on gene flow of intertidal species failed to be detected in some other cases [13]. Therefore, it is of great interest and importance to investigate the historical and contemporary interplay among a complex set of ecological, genetic, demographic, oceanographic and climatic processes in the coast of East Asia during Pleistocene glacial-interglacial cycles.…”

Significant genetic differentiation between the Yellow Sea and East China Sea populations of cocktail shrimp Trachypenaeus curvirostris revealed by the mitochondrial DNA COI gene

“…Freshwater discharge from the Yangtze River was thought to act as a physical barrier limiting the southward dispersal of larvae from Yellow Sea populations to the rest of the Chinese populations of C. toreuma. However, for other marine organism including fishes, crabs and molluscs in this region, there are few studies about significant genetic divergence in line with the outflow (reviewed in Ni et al, 2012). For example, Nibea albiflora, a member of the family Sciaenidae, widely distributes in the coastal waters of East China Sea and Yellow Sea.…”