The rainbow clam Moerella iridescens is an economically important small-sized marine clam due to its delicious taste and high nutritional value. The clam is mainly distributed on the West Pacific coast and northern Australia. In recent years, the rainbow clam has been increasingly used as high-valued seafood and is preferred by consumers of China, and the output of the rainbow clams mainly comes from marine fishing. However, in the past 2 years, the development of the shrimp and crab aquaculture industry and the overfishing of wild rainbow clams have exacerbated the destruction of the habitat of rainbow clams. Moreover, the status of genetic diversity of the germplasm resources of rainbow clams remains unclear. Thus, the protection of rainbow clam resources is of great importance. Several authors have explored the biological characteristics and morphological differences of rainbow clams (Ji et al., 2007; Lv et al., 2012). To date, however, reports on the genetic diversity and relationships among clam populations are limited (Xu et al., 2016).

Microsatellites, also known as simple repetitive sequences (SSRs), present the advantages of co-dominance, single locus, high polymorphism, and easy operation and can be screened from different populations to complete genetic diversity studies (Cui et al., 2011). Microsatellite marker technology has been widely used in the structural analysis of the population genetics of aquatic animals, e.g., the rainbow trout (Zhao et al., 2010), the scallop Patinopecten yessoensis (Chang et al., 2007), and the triangle pearl Hyriopsis cummingii (Bai et al., 2015). So far, few reports are available on the genetic diversity of the population of rainbow clams. In the present study, the genetic diversity of six populations of rainbow clams in Lianyungang, Chongming Island, Ningde, Zhoushan, Cixi, and Wenzhou was analyzed by using microsatellite markers. The results obtained can provide a scientific basis for assessing germplasm resources and genetic diversity protection of rainbow clams.

Genetic differentiation index (F_ST) is an important parameter for measuring the degree of genetic differentiation in a population. A large F_ST value indicates a high degree of differentiation between populations. No differentiation exists when F_ST is 0−0.05, moderate differentiation is observed when F_ST is 0.05−0.15, high differentiation is obtained when F_ST is 0.15−0.25, and great differentiation is found when F_ST > 0.25 (Hartl and Clark, 1997). In this study, the F_ST of the six populations under study was 0.047 (<0.05). Overall, the differentiation between the populations was minimal at best. However, the F_ST values of the ZS−LYG, ZS−CM, ZS−WZ, LYG−ND, and CM−ND populations were in the range of 0.0624−0.0790 (0.05), which indicates that moderate genetic differentiation existed between the Zhoushan and each of the Lianyungang, Chongming, and Wenzhou populations and between the Ningde and each of the Lianyungang and Chongming populations of rainbow clams. Nm can indicate the degree of genetic differentiation in a population. If Nm < 1, genetic differentiation occurs among populations. If Nm > 1, genetic differentiation is relatively low. If Nm > 4, genetic differentiation is very low (Ratnaningrum et al., 2017). The results of AMOVA showed that the Nm values among the six populations of rainbow clams lay between 2.9146 and 13.2635, and the Nm values among the ZS−LYG, ZS−CM, ZS–WZ, LYG−ND, and CM−ND populations were greater than 1 and less than 4. These results indicate low genetic differentiation among these populations. In the present study, the sampling area of rainbow clams was distributed in the Yellow Sea and East China Seas. LYG and CM are in the Yellow Sea with a geographical distance (about 1,000 km coastline), and no differentiation between these populations was observed (F_ST = 0.0040 < 0.05). Although the geographical distance between the Chongming and Zhoushan populations is close, the Yangtze estuary is situated between them. The inflow of the Yangtze River lowers the salinity of the seawater and, hence, obstructs the passage of larvae and hinders gene communication to some extent (the Nm for CM−ZS is 2.9146). Therefore, moderate genetic differentiation occurs between the CM and ZS populations (F_ST = 0.0790). Xu et al. (2016) analyzed the population morphology and genetic diversity of rainbow clams from Zhejiang and revealed that the Zhoushan population has great variation from the Yueqing, Taizhou, and Wenling populations (G_ST = 0.2479). The present study also indicated that genetic differentiation occurred in the Zhoushan population (F_ST = 0.2479), which was consistent with Xu et al. (2016), who showed that the Zhoushan population of rainbow clams presents moderate genetic differentiation.

This study also found that the degree of genetic differentiation between rainbow clam populations is not related to the geographical distance. Although the geographical distance between LYG and CX was relatively far away, the F_ST value between the LYG and CX populations of the rainbow was shallow, only 0.0180 (<0.05), which indicated a lack of genetic differentiation between the two populations. The gene exchange between the two populations occurred frequently (Nm = 13.2635 > 4). The inconsistency of the relationship between the degree of genetic differentiation and geographical distance has previously been observed in different populations of Coelomactra antiquata. Meng et al. (2013) showed that the population genetic differentiation between the C. antiquata from the Southeastern Sea and that from the Yellow Sea in Lianyungang and Rizhao is not apparent based on the results of ITS2 and 16S rRNA for six populations of C. antiquata in the coasts of China. By contrast, the difference between the Guangxi and Fujian populations, which have a relatively close geographical distance, reached the interspecies level. The real reason may be from human activity, such as artificial farming and introduction, but more detailed reasons remain unknown so far.

Genetic diversity, including the degree of genetic variation and the genetic structure of the population, is an important basis for evaluating the status of genetic resources. A higher genetic diversity of a population results in a stronger adaptability to the living environment and a greater potential for evolution (Tian et al., 2013). The genetic diversity of a population is mainly manifested in two aspects: heterozygosity and the number of alleles (Yu et al., 2012). Many reports have explored the genetic diversity of aquatic animals by using SSR markers. Li et al. (2011) studied the population genetics of Portunus trituberculatus by microsatellite markers and found an average Ho of 0.2222−1.0000 and an average He of 0.4367−0.9099. Li et al. (2009) used SSR technology to measure the average Ho (0.32−0.49) of wild and cultured populations of scallops and found an average He of 0.37−0.55. Chang et al. (2007) analyzed the genetic diversity of five populations of scallops P. yessoensis in China and abroad and found an average Ho of 0.2708−0.3292 and an average He of 0.3620−0.4595 for the five populations. Tian et al. (2013) determine the Ho and He of four populations of Scapharca broughtonii by using the 20 microsatellite markers, and the results showed that the ranges of Ho and He was 0.667–0.9667 and 0.6198–0.9318, respectively. An et al. (2012) studied the genetic structure of five wild-type populations of Ruditapes philippinarum in two sea areas of Korea by using seven SSR markers and noted high genetic diversity among the clams (total He = 0.813). The results of the present study revealed that the average Ho of the six populations of rainbow clam was between 0.4381 and 0.6139 and that the He was 0.6266−0.7325. Specifically, the value of He was as follows: ZS (0.7325), CX (0.7162), ND (0.6839), LYG (0.6786), CM (0.6701), and WZ (0.6266). The average number of alleles of the 17 loci in the six populations ranged from 5.5000 to 22.500, and the Ne was between 1.2538 and 13.3411. The genetic diversity of the rainbow clams was higher than those of bay scallop Argopecten irradians and scallop P. yessoensis. This particular genetic diversity is similar to the He of four populations of clams T. quinquefasciatus and is lower than that of five populations of clam R. philippinarum. Generally, the He (0.7325) of the present study and Shannon diversity index (1.7998) were the highest in the Zhoushan population, which indicated that the Zhoushan population has the richest genetic diversity among the clam populations studied.

The population differentiation of the existing rainbow clams is not obvious, and the genetic diversity of germplasm resources is relatively high, indicating that the effective population of rainbow clams in nature is large enough. At present, it is not very urgent to establish a germplasm resource reserve and its ex situ culture technology. In the future, the monitoring and evaluation of the germplasm resources of rainbow clams should be strengthened.

The six populations of rainbow clams all presented high genetic diversity, which reflect the good protection and development prospects of rainbow clam resources in China. These results would be helpful to genetic breeding practice and resources management.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

All applicable International, National, and/or Institutional Guidelines for the Care and Use of Animals (invertebrates) were followed.

XL conceived and designed the experiments. SG performed the experiments. MZ analyzed the data. XL and ZD wrote the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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