The population history of Garra orientalis (Teleostei: Cyprinidae) using mitochondrial DNA and microsatellite data with approximate Bayesian computation

Abstract

Background: The South China landmass has been characterized by a complex geological history, including mountain lifting, climate changes, and river capture/reversal events. To determine how this complexity has influenced the landmass's phylogeography, our study examined the phylogeography of Garra orientalis, a cyprinid widely distributed in South China, using sequences from the mitochondrial DNA control region and cytochrome b gene (1887 bp) and polymorphisms of thirteen microsatellite loci.

Results: In total, 157 specimens were collected from eight populations. All 88 mtDNA haplotypes were identified as belonging to three major lineages, and these lineages were almost allopatric in their distributions. The results of a statistical dispersal-vicariance analysis suggested that the ancestral populations of G. orientalis were distributed south of the Yunkai Mountains, including on Hainan Island. The mtDNA data revealed a strong relationship between phylogeny and geography. In the microsatellite analysis, a total of 339 alleles with an average of 26 alleles per locus were observed across thirteen microsatellite loci. A clustering algorithm for microsatellite data revealed an admixture-like genetic structure. Although the mtDNA and microsatellite data sets displayed a discordant population structure, the results of an approximate Bayesian computation approach showed that these two markers revealed congruent historical signals. The population history of G. orientalis reflects vicariance events and dispersal related to the complex geological history of South China.

Conclusion: Our results (i) found that the discordances between mtDNA and microsatellite markers were accounted for by admixtures; (ii) showed that the Wuzhishan and Yinggeling mountain ranges and Qiongzhou Strait were important barriers limiting gene exchange between populations on both sides; (iii) indicated that during glaciation and inter-glacial periods, the strait and continental shelves were exposed and sank, which contributed with the dispersion and differentiation of populations; and (iv) displayed that the admixtures between lineages took place in coastal populations and then colonized the tributaries of the Pearl River.

Keywords: Approximate Bayesian computation; Garra orientalis; Microsatellite; Mitochondria; Phylogeography.

Fig. 1

Sampling localities of Garra orientalis are indicated by ●. The ichthyofaunal districts were defined by Li (1981)

Fig. 2

Phylogenetic analysis based on mitochondrial DNA cytochrome b and D-loop sequences. a The ML tree with HKY model. The numbers at the nodes are bootstrap values of the ML, NJ and BI analyses. The haplotype network b and the distribution of the major mtDNA lineages c

Fig. 3

STRUCTRUE and NJ trees based on microsatellite data. a The frequency of inferred population clusters with the program STRUCTURE. Membership coefficients inferred for K = 4. Each of the inferred population clusters is represented by a color. b The NJ tree, visualizing genetic distances among the inferred clusters. c The NJ tree of genetic relationships among eight populations using D_A genetic distance. d The distribution of groups revealed in the NJ tree

Fig. 4

Graphical representation of the five scenarios, a null hypotheses, b mtDNA phylogenetic model, c mtDNA S-DIVA model, d microsatellite phylogenetic model, and e microsatellite STRUCTURE model, used in the ABC analyses. N values are population sizes, and t values correspond to the timing of past divergence events or past admixture between populations. Note that time is not to scale

Fig. 5

The colonization history of Garra orientalis. The blue area indicates the distribution of ancestral populations a, and b-c the orange, green and purple are the distributions of mtDNA lineages I-III in Fig. 2, respectively. d The lineages I(purple) and II (green) were admixed in coastal populations and then migrated from coastral populations to lower and upper tributaries of the Pearl River