Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus

Abstract

BackgroundThe study of speciation in the marine realm is challenging because of the apparent absence of physical barriers to dispersal, which are one of the main drivers of genetic diversity. Although phylogeographic studies using mitochondrial DNA (mtDNA) information often reveal significant genetic heterogeneity within marine species, the evolutionary significance of such diversity is difficult to interpret with these markers. In the northwestern (NW) Pacific, several studies have emphasised the potential importance of sea-level regression during the most recent glaciations as a driver of genetic diversity in marine species. These studies have failed, however, to determine whether the period of isolation was long enough for divergence to attain speciation. Among these marine species, the cosmopolitan estuarine-dependent fish Mugil cephalus represents an interesting case study. Several divergent allopatric mtDNA lineages have been described in this species worldwide, and three occur in sympatry in the NW Pacific.ResultsTen nuclear microsatellites were surveyed to estimate the level of genetic isolation of these lineages and determine the role of sea-level fluctuation in the evolution of NW Pacific M. cephalus. Three cryptic species of M. cephalus were identified within this region (NWP1, 2 and 3) using an assignment test on the microsatellite data. Each species corresponds with one of the three mtDNA lineages in the COI phylogenetic tree. NWP3 is the most divergent species, with a distribution range that suggests tropical affinities, while NWP1, with a northward distribution from Taiwan to Russia, is a temperate species. NWP2 is distributed along the warm Kuroshio Current. The divergence of NWP1 from NWP2 dates back to the Pleistocene epoch and probably corresponds to the separation of the Japan and China Seas when sea levels dropped. Despite their subsequent range expansion since this period of glaciation, no gene flow was observed among these three lineages, indicating that speciation has been achieved.ConclusionsThis study successfully identified three cryptic species in M. cephalus inhabiting the NW Pacific, using a combination of microsatellites and mitochondrial genetic markers. The current genetic architecture of the M. cephalus species complex in the NW Pacific is the result of a complex interaction of contemporary processes and historical events. Sea level and temperature fluctuations during Plio-Pleistocene epochs probably played a major role in creating the marine species diversity of the NW Pacific that is found today.

Population structure of Hirundichthys oxycephalus in the northwestern Pacific inferred from mitochondrial cytochrome oxidase I gene

“…However, the interrelationship of either stock to any sampling locality, the Kuroshio, or other minor currents was not detected. Similar results have also been observed in other marine fishes in the northwestern Pacific (Chiou and Lee 2004;Liu et al 2007;Han et al 2008a,b;Liu et al 2009;Wu et al 2009;Han et al 2010;Iida et al 2010;Shen et al 2011;Chu et al 2012;Ju et al 2013), in which major ocean current patterns are not good predictors of gene flow. On the other hand, historical factors such as Pleistocene glaciations might account for the genetic pattern of H. oxycephalus.…”

“…Similar observations were noted for some marine fauna, such as mitten crab, mottled spinefoot, and ice goby in the western Pacific, whose Bayesian skyline plots also indicated that the populations had experienced Pleistocene demographic expansion (Xu et al 2009;Ravago-Gotanco and Juinio-Meñez 2010;Kokita and Nohara 2011). In addition, the TMRCA estimates for all samples of H. oxycephalus indicated that the expansion occurred approximately in the middle Pleistocene period, which is much later than the flathead mullet in this region which occurred in the early Pleistocene period or even in the Pliocene period (Shen et al 2011). The low genetic differentiation among six localities in the northwestern Pacific Ocean, along with the variation mostly found within populations rather than among them (AMOVA , Table 2), implies a high gene flow of H. oxycephalus among populations.…”

“…The strong and constant Kuroshio Current might facilitate the gene flow of species distributed within the northwestern Pacific Ocean and result in a weak genetic structure (Hohenlohe 2004). This may account for the low genetic differentiation of H. oxycephalus and the other species distributed in the range of the Kuroshio Current, including albacore (Wu et al 2009), Japanese eel (Han et al 2010), Japanese anchovy (Liu et al 2006), crocker (Han et al 2008a,b), mackerel (Chiou and Lee 2004), mullet (Liu et al 2007;Liu et al 2009;Shen et al 2011), goby (Iida et al 2010;Ju et al 2013), and whiskered velvet shrimp (Chu et al 2012).…”

Effects of climate variability and climate change on the fishing conditions for grey mullet (Mugil cephalus L.) in the Taiwan Strait

“…These changes indicate that the strengthening of the NCCC in the TS weakened in winter because of the increased SSTs. Shen et al (2011) indicated that the regional group of grey mullet belonging to the NCCC might provide a particularly good indicator species for global warming. Our results demonstrate that grey mullet catches exhibited a decreasing trend after 1984, and the fishing ground shifted north following the northward shift of the 20°C isotherm.…”

“…Shen et al (2011) identified three cryptic species of M. cephalus in the northwestern Pacific Ocean and indicated that the distributional range of these species appeared to be governed primarily by three major ocean current systems, the South China Current, North China Coastal Current (NCCC), and Kuroshio Current. Previous studies have reported that the spawning and nursery grounds of the regional group of grey mullet affected by the NCCC are distributed in the coastal waters of the southeastern Taiwan Strait (TS).…”