Population genetic studies revealed local adaptation in a high gene-flow marine fish, the small yellow croaker (Larimichthys polyactis)

Abstract

The genetic differentiation of many marine fish species is low. Yet local adaptation may be common in marine fish species as the vast and changing marine environment provides more chances for natural selection. Here, we used anonymous as well as known protein gene linked microsatellites and mitochondrial DNA to detect the population structure of the small yellow croaker (Larimichthys polyactis) in the Northwest Pacific marginal seas. Among these loci, we detected at least two microsatellites, anonymous H16 and HSP27 to be clearly under diversifying selection in outlier tests. Sequence cloning and analysis revealed that H16 was located in the intron of BAHCC1 gene. Landscape genetic analysis showed that H16 mutations were significantly associated with temperature, which further supported the diversifying selection at this locus. These marker types presented different patterns of population structure: (i) mitochondrial DNA phylogeny showed no evidence of genetic divergence and demonstrated only one glacial linage; (ii) population differentiation using putatively neutral microsatellites presented a pattern of high gene flow in the L. polyactis. In addition, several genetic barriers were identified; (iii) the population differentiation pattern revealed by loci under diversifying selection was rather different from that revealed by putatively neutral loci. The results above suggest local adaptation in the small yellow croaker. In summary, population genetic studies based on different marker types disentangle the effects of demographic history, migration, genetic drift and local adaptation on population structure and also provide valuable new insights for the design of management strategies in L. polyactis.

Figure 1. Map of sampling localities and allele frequencies at locus H16.

Sample numbers match those in Table 1. Pie charts denote allele frequencies at H16, in which each color represents one allele identity. Well supported and less well supported barriers to gene flow based on neutral microsatellites are also shown with broken lines that are proportional to replicates support. The sea areas are shown in abbreviations corresponding to Table 1. The southward China Coastal Cold Current and northward Taiwan Warm Current are also shown with arrows.

Figure 2. Results of the outlier tests using BAYESCAN.

Loci identified as significant outliers under the decisive criterion of Jeffrey’s interpretation are denoted as solid circles.

Figure 3. Results of the outlier tests using LOSITAN (outliers are above the 99% confidence interval curve) and under hierarchical island model using Arlequin (H16 and HSP27 are still outliers, whereas H51 and H65 lost significance as outliers).

Figure 4. PCA plotting of population differentiation based on (a) neutral microsatellites; (b) locus H16; (c) locus HSP27.

Figure 5. Plotting results of the program STRUCTURE for neutral loci with K ranging from 3 to 5 and for whole data set with K from 2 to 4, respectively.

Sample identities and its corresponding geographical regions are also showed.