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Complex population genetic and demographic history of the Salangid, Neosalanx taihuensis, based on cytochrome b sequences.

Zhao L, Zhang J, Liu Z, Funk SM, Wei F, Xu M, Li M - BMC Evol. Biol. (2008)

Bottom Line: This wide ranging distribution makes the species an ideal model for the study of palaeoclimatic effects on population genetic structure and phylogeography.The most common haplotype (H36) was found in 49.15% of all individuals.The observed complex genetic pattern of N. taihuensis is coherent with a scenario of multiple unrelated founding events by long-distance colonization and dispersal combined with contiguous population expansion and locally restricted gene flow.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Chaoyang, Beijing 100101, PR China. zhaoliang@ioz.ac.cn

ABSTRACT

Background: The Salangid icefish Neosalanx taihuensis (Salangidae) is an economically important fish, which is endemic to China, restricted to large freshwater systems (e.g. lakes, large rivers and estuaries) and typically exhibit low vagility. The continuous distribution ranges from the temperate region of the Huai and Yellow River basins to the subtropical region of the Pearl River basin. This wide ranging distribution makes the species an ideal model for the study of palaeoclimatic effects on population genetic structure and phylogeography. Here, we aim to analyze population genetic differentiation within and between river basins and demographic history in order to understand how this species responded to severe climatic oscillations, decline of the sea levels during the Pleistocene ice ages and tectonic activity.

Results: We obtained the complete mtDNA cytochrome b sequences (1141 bp) of 354 individuals from 13 populations in the Pearl River, the Yangze River and the Huai River basin. Thirty-six haplotypes were detected. Haplotype frequency distributions were strongly skewed, with most haplotypes (n = 24) represented only in single samples each and thus restricted to a single population. The most common haplotype (H36) was found in 49.15% of all individuals. Analysis of molecular variance (AMOVA) revealed a random pattern in the distribution of genetic diversity, which is inconsistent with contemporary hydrological structure. Significant levels of genetic subdivision were detected among populations within basins rather than between the three basins. Demographic analysis revealed that the population size in the Pearl River basin has remained relatively constant whereas the populations in the Yangze River and the Huai River basins expanded about 221 and 190 kyr ago, respectively, with the majority of mutations occurring after the last glacial maximum (LGM).

Conclusion: The observed complex genetic pattern of N. taihuensis is coherent with a scenario of multiple unrelated founding events by long-distance colonization and dispersal combined with contiguous population expansion and locally restricted gene flow. We also found that this species was likely severely impacted by past glaciations. More favourable climate and the formation of large suitable habitations together facilitated population expansion after the late Quaternary (especially the LGM). We proposed that all populations should be managed and conserved separately, especially for habitat protection.

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Observed and expected mismatch distributions showing the frequencies of pairwise differences. The observed distributions (bars) are compared for their goodness-of-fit to a Poisson distribution under a model of sudden expansion illustrated by the overlaid curve (black dots and solid lines). X-axis: number of pair-wise differences, Y-axis: frequency.
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Figure 5: Observed and expected mismatch distributions showing the frequencies of pairwise differences. The observed distributions (bars) are compared for their goodness-of-fit to a Poisson distribution under a model of sudden expansion illustrated by the overlaid curve (black dots and solid lines). X-axis: number of pair-wise differences, Y-axis: frequency.

Mentions: An examination of demographic histories revealed the marked differences among the basins under study (Table 5, Figure 4, Figure 5). The skyline plots [38,39]of N. taihuensis in the entire region and the Yangze River basin showed a sudden stepwise expansion. Fu's Fs [40], Ramos-Onsins and Rozas's R2 [41] tests for the entire region and Fu's Fs test for Yangze River basin were statistically significant negative, supported this point. Although both Fs and R2 tests could not effectively tell the causes of bottleneck or expansion, Fu and Li's D* [42] tests were not significant (P > 0.05) for these populations, suggesting that there were no historical reduction in effective population size in these regions. The mtDNA mismatch analyses for the entire region and the Yangze River basin showed bimodal profile which might result from constant population size among an old population or an admixture population (Figure 5). However, the mismatch distribution goodness of fit test (Table 5) was not significant, which indicated that there were no severe departure from the estimated demographic model. Moreover, the results of the coalescent based analysis using FLUCTUATE1.4 [43] showed high growth rate, g = 2648.97 ± 556.26 for the entire region and g = 3268.21 ± 873.30 for the Yangze River basin, providing powerful evidences of population expansion in these regions. In contrast to that of the entire region and the Yangze River basin, the skyline plot for Huai River basin provided evidence that the exponential growth model fitted the population demographic fluctuation well (Figure 4). Significant Fu's Fs (P <0.05) and Ramos-Onsins and Rozas's R2 (P < 0.05) test, as well as high growth rate (g = 2083.14 ± 529.35) confirmed population growth in Huai River basin, which was also supported by the test of Hri (P > 0.95), although the bimodal mismatch distribution (Figure. 5) and significance of SSD (P < 0.05) indicated a poor fit for the stepwise growth model (Table 5). For the Pearl River basin, the bimodal mismatch distribution (Figure. 5) and significance of SSD (P < 0.05) values indicated a relative constant population size. Fu and Li's D* test, Fu's Fs and R2 test for Pearl River basin were not significant, which also rejected population expansion/bottleneck model (Table 5). In addition, a relative constant population size was confirmed by a relative low growth rate (g = -309.64 ± 955.56) with the approximate 95% confidence interval of g included zero in this region.


Complex population genetic and demographic history of the Salangid, Neosalanx taihuensis, based on cytochrome b sequences.

Zhao L, Zhang J, Liu Z, Funk SM, Wei F, Xu M, Li M - BMC Evol. Biol. (2008)

Observed and expected mismatch distributions showing the frequencies of pairwise differences. The observed distributions (bars) are compared for their goodness-of-fit to a Poisson distribution under a model of sudden expansion illustrated by the overlaid curve (black dots and solid lines). X-axis: number of pair-wise differences, Y-axis: frequency.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2483725&req=5

Figure 5: Observed and expected mismatch distributions showing the frequencies of pairwise differences. The observed distributions (bars) are compared for their goodness-of-fit to a Poisson distribution under a model of sudden expansion illustrated by the overlaid curve (black dots and solid lines). X-axis: number of pair-wise differences, Y-axis: frequency.
Mentions: An examination of demographic histories revealed the marked differences among the basins under study (Table 5, Figure 4, Figure 5). The skyline plots [38,39]of N. taihuensis in the entire region and the Yangze River basin showed a sudden stepwise expansion. Fu's Fs [40], Ramos-Onsins and Rozas's R2 [41] tests for the entire region and Fu's Fs test for Yangze River basin were statistically significant negative, supported this point. Although both Fs and R2 tests could not effectively tell the causes of bottleneck or expansion, Fu and Li's D* [42] tests were not significant (P > 0.05) for these populations, suggesting that there were no historical reduction in effective population size in these regions. The mtDNA mismatch analyses for the entire region and the Yangze River basin showed bimodal profile which might result from constant population size among an old population or an admixture population (Figure 5). However, the mismatch distribution goodness of fit test (Table 5) was not significant, which indicated that there were no severe departure from the estimated demographic model. Moreover, the results of the coalescent based analysis using FLUCTUATE1.4 [43] showed high growth rate, g = 2648.97 ± 556.26 for the entire region and g = 3268.21 ± 873.30 for the Yangze River basin, providing powerful evidences of population expansion in these regions. In contrast to that of the entire region and the Yangze River basin, the skyline plot for Huai River basin provided evidence that the exponential growth model fitted the population demographic fluctuation well (Figure 4). Significant Fu's Fs (P <0.05) and Ramos-Onsins and Rozas's R2 (P < 0.05) test, as well as high growth rate (g = 2083.14 ± 529.35) confirmed population growth in Huai River basin, which was also supported by the test of Hri (P > 0.95), although the bimodal mismatch distribution (Figure. 5) and significance of SSD (P < 0.05) indicated a poor fit for the stepwise growth model (Table 5). For the Pearl River basin, the bimodal mismatch distribution (Figure. 5) and significance of SSD (P < 0.05) values indicated a relative constant population size. Fu and Li's D* test, Fu's Fs and R2 test for Pearl River basin were not significant, which also rejected population expansion/bottleneck model (Table 5). In addition, a relative constant population size was confirmed by a relative low growth rate (g = -309.64 ± 955.56) with the approximate 95% confidence interval of g included zero in this region.

Bottom Line: This wide ranging distribution makes the species an ideal model for the study of palaeoclimatic effects on population genetic structure and phylogeography.The most common haplotype (H36) was found in 49.15% of all individuals.The observed complex genetic pattern of N. taihuensis is coherent with a scenario of multiple unrelated founding events by long-distance colonization and dispersal combined with contiguous population expansion and locally restricted gene flow.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Chaoyang, Beijing 100101, PR China. zhaoliang@ioz.ac.cn

ABSTRACT

Background: The Salangid icefish Neosalanx taihuensis (Salangidae) is an economically important fish, which is endemic to China, restricted to large freshwater systems (e.g. lakes, large rivers and estuaries) and typically exhibit low vagility. The continuous distribution ranges from the temperate region of the Huai and Yellow River basins to the subtropical region of the Pearl River basin. This wide ranging distribution makes the species an ideal model for the study of palaeoclimatic effects on population genetic structure and phylogeography. Here, we aim to analyze population genetic differentiation within and between river basins and demographic history in order to understand how this species responded to severe climatic oscillations, decline of the sea levels during the Pleistocene ice ages and tectonic activity.

Results: We obtained the complete mtDNA cytochrome b sequences (1141 bp) of 354 individuals from 13 populations in the Pearl River, the Yangze River and the Huai River basin. Thirty-six haplotypes were detected. Haplotype frequency distributions were strongly skewed, with most haplotypes (n = 24) represented only in single samples each and thus restricted to a single population. The most common haplotype (H36) was found in 49.15% of all individuals. Analysis of molecular variance (AMOVA) revealed a random pattern in the distribution of genetic diversity, which is inconsistent with contemporary hydrological structure. Significant levels of genetic subdivision were detected among populations within basins rather than between the three basins. Demographic analysis revealed that the population size in the Pearl River basin has remained relatively constant whereas the populations in the Yangze River and the Huai River basins expanded about 221 and 190 kyr ago, respectively, with the majority of mutations occurring after the last glacial maximum (LGM).

Conclusion: The observed complex genetic pattern of N. taihuensis is coherent with a scenario of multiple unrelated founding events by long-distance colonization and dispersal combined with contiguous population expansion and locally restricted gene flow. We also found that this species was likely severely impacted by past glaciations. More favourable climate and the formation of large suitable habitations together facilitated population expansion after the late Quaternary (especially the LGM). We proposed that all populations should be managed and conserved separately, especially for habitat protection.

Show MeSH
Related in: MedlinePlus