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Demographic response of cutlassfish (Trichiurus japonicus and T. nanhaiensis) to fluctuating palaeo-climate and regional oceanographic conditions in the China seas

Glacial cycles of the Quaternary have heavily influenced the demographic history of various species. To test the evolutionary impact of palaeo-geologic and climatic events on the demographic history of marine taxa from the coastal Western Pacific, we investigated the population structure and demographic history of two economically important fish (Trichiurus japonicus and T. nanhaiensis) that inhabit the continental shelves of the East China and northern South China Seas using the mitochondrial cytochrome b sequences and Bayesian Skyline Plot analyses. A molecular rate of 2.03% per million years, calibrated to the earliest flooding of the East China Sea shelf (70–140 kya), revealed a strong correlation between population sizes and primary production. Furthermore, comparison of the demographic history of T. japonicus populations from the East China and South China Seas provided evidence of the postglacial development of the Changjiang (Yangtze River) Delta. In the South China Sea, interspecific comparisons between T. japonicus and T. nanhaiensis indicated possible evolutionary responses to changes in palaeo-productivity that were influenced by East Asian winter monsoons. This study not only provides insight into the demographic history of cutlassfish but also reveals potential clues regarding the historic productivity and regional oceanographic conditions of the Western Pacific marginal seas.


Supplementary Information S1: Molecular clock variation and calibration
Sequence substitution rates of the mitochondrial Cyt b gene of fish have been shown to vary greatly between species. For example, molecular rates of 0.34%/myr (Cobitis) (Doadrio & Perdices, 2005), 0.53-0.66%/myr (Plagopterini and Barbus) (Dowling et al., 2002;Tsigenopoulos et al., 2003), and 0.9-1.2%/myr (cichlid and schizothoracine fishes) (Martin & Bermingham, 1998;He et al., 2004) have all recently been reported. However, molecular rate calibrations, such as these, based on interspecific phylogenetic divergence, geologic and/or fossils evidence have been shown to be unreliable and often underestimate actual divergence due to purifying selection or mutational hot spots (Ho et al., 2005;Burridge et al., 2008). Furthermore, recent studies have shown that short-term mtDNA evolutionary rates are elevated relative to long-term (deeper phylogenetic level) rates (Santos et al., 2005;Kemp et al., 2007;Crandall et al., 2012). The present study indeed presents an elevated molecular rate estimation of 2.03 (1.35-2.7)%/myr for Trichiurus calibrated to the earliest inundation on the newly formed wide East China Sea shelf (150 kya) by rising sea level of the last interglacial period (70~140 kya).

Supplementary Information S2: Geological history of the China seas
The last uplift of the Tibetan Plateau, occurring around 150 kya (Sun et al., 2003), accompanied by the costal subsidence of East China is thought to have created wide and flat continental shelves in the East China Sea and northern South China Sea . However, the absence of marine deposits during the early and middle Pleistocene suggest that these continental shelves were much narrower and steeper prior to this event (Wang et al., 1981;1985).

China Sea and South China Sea influenced by the rivers and monsoon
The large differences in the influx of freshwater and terrigenous sediment between the East China Sea and northern South China Sea likely resulted in different primary productivities of these two seas. For example, the Changjang (Yangtze River) introduces nearly 9.54×10 11 m 3 of freshwater and 5×10 8 tons of sediment into the East China Sea per year (Wang et al., 1988); whereas as the second largest river in China, the Pearl River, only provides 3.03×10 11 m 3 of freshwater and 0.89×10 8 tons of sediment into the South China Sea per year (Wei & Wu, 2011;Yang et al., 2011).
Furthermore, the primary production of the present day northern South China Sea in summer is much lower than that in winter due to nutrient advection constraint by summer shallow thermoclines and weak vertical mixing (Tang et al., 2003;Chen et al., 2006), which suggest that coastal river discharge plays a less important role relative to winter monsoons in influencing the primary production of the northern South China Sea.

Supplementary Information S4: Geological history of the Changjiang
Historically, the Changjiang is thought to have drained into the East China Sea since the late Pleistocene (Zhu et al., 1984;Li & Zhang, 1995). However, given the absence of Changjiang derived sediments on the ECS shelf prior to the Holocene and the decrease in salinity of the Japan Sea during the LGM, some believe the palaeo-Changjiang historically drained into the Japan Sea or did not enter the East China Sea until the Holocene (Zhao et al., 1983;Zhong et al., 1983;Zhao, 1984;Yang, 1991).

Supplementary Information S5: Interspecific competition between T. japonicus and T. nanhaiensis
The continuous population growth of T. japonicus compared to the population contraction of T. nanhaiensis prior to 37.5 kya observed in the northern South China Sea (Fig. 5) might be attributed to limited niche space and/or inter-specific competition. In terms of dietary needs, habitat space and resource partitioning, T. japonicus and T. nanhaiensis have similar niche requirements (Lin et al., 2005;Yan et al., 2010). In this context, the larger population size of T. japonicus over the last 165 kya may have allowed it to successfully occupy much of the available niche space of the northern South China Sea and outcompete species of lower abundance like T. nanhaiensis (Fig. 5). With the continued population expansion of T. japonicus and increased interspecific competition this brought, the population size of T. nanhaiensis steadily declined from 165 to 37.5 kya (Fig. 5).

Supplementary Information S6: Palao-productivity influenced by winter monsoon in the northern Southern China Sea
Primary production in the northern South China Sea was mainly influenced by the winter monssons. For example, present or palaeo-productivity increased due to high nutrient input from upwelling and terrestrial deposits caused by the intense winter monsoons in the northern South China Sea during winter or periods of glaciations ( Fig. 5) and decreased due to low nutrient input by shallow mixing layers during summer or weaker winter monsoons during interglacial periods (Li et al., 2002;Tang et al., 2003;Li & Wang, 2004;Chen & Chen, 2006;Wang et al., 2007).

Supplementary Information S7: Link between East Asian monsoons and population dynamics in the China seas
In the East China Sea, a general link between interglacial intensified summer monsoons, increased precipitation followed by high nutrient input from the Changjiang, high primary production and population expansions was revealed.