Elsevier

Gene Reports

Volume 23, June 2021, 101047
Gene Reports

Genetic diversity and population structure of wild and domesticated black tiger shrimp (Penaeus monodon) broodstocks in the Indo-Pacific regions using consolidated mtDNA and microsatellite markers

https://doi.org/10.1016/j.genrep.2021.101047Get rights and content

Highlights

  • Genetic diversity of Penaeus monodon were analyzed by mtDNA and microsatellite markers

  • Microsatellite DNA data were observed to be concordant with the mtDNA dataset

  • Domesticated populations were unequivocally diverged from the wild populations

  • These findings are useful for sustainable management and domestication of P. monodon broodstocks

Abstract

Black tiger shrimp (Penaeus monodon) is one of the most important internationally traded fishery species, and the commercial success of their aquafarming primarily depends on the high quality broodstock for seed production. Therefore, identifications of genetically diverse broodstocks of P. monodon are essential to eliminate inbreeding effects, ensure sustainable seed supply, and facilitate genetic upgrading for selective breeding and restocking programs. The present study used a combination of mtDNA control region sequences and ten microsatellite markers to evaluate the genetic diversity, demographic history and population structure of P. monodon broodstocks collected from five sampling locations across the Indo-Pacific regions. The domesticated P. monodon broodstock populations were collected from Hawaii, USA (MMO), Thailand (MT) and Madagascar (MD), while the wild broodstock populations were collected from Japan (MJ) and Malaysia (MS). Clustering analyses based on the Principle Component Analysis (PCA), Canonical Variate Analysis (CVA), STRUCTURE, and Neighbour-Joining (NJ) phylogenetic analysis revealed that the domesticated populations were unequivocally diverged from the wild-caught populations. Haplotype networks, neutrality testing, and mismatch distribution analysis indicated a complex population expansion pattern involving Wahlund effect based on human translocation, and continental drift during the paleogeographic event in Pleistocene glacial age. Both mtDNA and microsatellite data detected relatively high levels of genetic diversity among all populations, but higher levels of nucleotide diversity in the wild populations, given that the artificial selection in aquaculture practice could reduce the genetic heterogeneity of the domesticated populations. The negative correlation of isolation by distance (IBD) results further supported the findings from neutrality test, indicating that founder stocks for genetic improvement program which were established from several geographic origins may have caused admixture in the domesticated populations. The genetic information obtained from this study could help to establish appropriate breeding strategies and genetic improvement program, and would provide essential data for genetic management and conservation of P. monodon wild populations.

Introduction

The giant black tiger shrimp, Penaeus monodon is distributed worldwide in the Indo-West Pacific region, and has been commercially cultured to meet the increased global seafood market demand (Mohamed, 1970; Holthuis, 1980). This species has been extensively farmed for more than decade in various regions within its native habitats, in which the wild broodstocks were sought after initially for the domestication programs (Rosenberry, 2001; Benzie et al., 2002; You et al., 2008; Azad et al., 2009; Mandal et al., 2012; Waqairatu et al., 2012; Vaseeharan et al., 2013; Alam et al., 2016). The high reliance on the wild-caught spawners for seed production result in over-exploitation of the natural populations, affecting the sustainability and biodiversity of fishery resources (Hulata, 2001; Klinbunga et al., 2001; Kumar et al., 2007). Indeed, the fluctuations in the availability and quality of the wild broodstocks warrant the need in developing genetic improvement and selective breeding program for the shrimp industry (Benzie, 1998; Jarayabhand et al., 1998; Withyachumnarnkul et al., 1998). Therefore, identification of genetically diverse and geographically differentiated wild shrimp broodstocks will be essential to ensure sustainable seed supply, eliminate inbreeding effects, and facilitate genetic upgrading for both selective breeding and restocking programs of P. monodon (Kumar et al., 2007).

Besides the wild broodstock populations, shrimp farming is also profoundly reliant on seed production from the domesticated broodstocks (Klinbunga et al., 2001). The loss of genetic diversity could reduce the adaptability of the species to environmental changes (Liu et al., 2013) which has also been reported during domestication process (Dixon et al., 2008; De Donato et al., 2005). In many countries, using of low number of breeders and/or mass or unintended selection of prospective domesticated broodstock populations often resulted in a decrease of effective population size, loss of genetic discrimination, and build-up of inbreeding effects over subsequent generations (De Donato et al., 2005; Dixon et al., 2008; Khedkar et al., 2013). Moreover, the general mean phenotypic value of traits associated with reproductive fitness and physiological efficiencies are also often reduced, although the extent of such effects are variable between various traits and species (Hedrick and Kalinowski, 2000; Ponzoni et al., 2010). Therefore, preserving sufficient levels of genetic diversity in domesticated broodstock populations are essential for the gene pool conservation in cultured shrimp (Rezaee et al., 2015). Long-term and sustainable crossbreeding programs of domesticated shrimp broodstock populations may benefit to attain the stability between unceasing genetic gains and reduced risk of inbreeding depression (Zhang et al., 2010; Ríos-Pérez et al., 2017). Since last few decades, various techniques used in examining genetic diversity status of P. monodon ranged from the most traditional allozymes (Benzie et al., 1992, Benzie et al., 1993; Forbes et al., 1999; Sugama et al., 2002)), randomly amplified polymorphic DNA (Garcia and Benzie, 1995; Tassanakajon et al., 1997, Tassanakajon et al., 1998; Klinbunga et al., 2001), elongation factor 1-a intron sequences (Duda and Palumbi, 1999), restriction fragment length polymorphism (RFLP) (Benzie et al., 1993, Benzie et al., 2002; Bouchon et al., 1994; Klinbunga et al., 1998, Klinbunga et al., 2001), mitochondrial DNA sequencing (Chu et al., 2002; Kumar et al., 2007; You et al., 2008; Khamnamtong et al., 2009; Waqairatu et al., 2012; Khedkar et al., 2013; Alam et al., 2016) to microsatellites (Wolfus et al., 1997; Xu et al., 1999, Xu et al., 2001; Brooker et al., 2000; Supungul et al., 2000; Wuthisuthimethavee et al., 2003; Pan et al., 2004; Li et al., 2007; Dixon et al., 2008; You et al., 2008; Aziz et al., 2011; Mandal et al., 2012; Waqairatu et al., 2012). Among these techniques, microsatellite markers are promising in studying population genetic variability owing to their broad genome distribution of codominant polymorphisms, high reproducibility, convenient detection (Varshney et al., 2005; Presti and Wasko, 2014). They are powerful in estimating gene flow pattern, recent expansion and historical colonization even among closely related populations sampled over reduced geographical scale (Wright and Bentzen, 1994; Estoup et al., 1993). On the other hand, the effective population size measured by mtDNA is generally smaller than that of nuclear markers such as allozyme and nuclear DNA (Birky et al., 1989), due to its maternal inheritance, no genetic recombination of intermolecular, high susceptibility to genetic drift effects, and rapid evolutionary rate (Filipova et al., 2011; Xu et al., 2009). This allows mtDNA to possess sharper genetic differentiation and increased sensitivity to inbreeding and bottleneck effects (O'Connell et al., 1998). Taken together, with the evidence from previous studies, the consolidated use of mtDNA and microsatellite markers would greatly improve the overall detectability of genetic diversity in many aquatic species (Sekino et al., 2002; Li et al., 2016).

Genetic diversity studies of P. monodon have been conducted at both microgeographic and macrogeographic levels using various molecular markers. The microgeographic scale studies were limited to one region/country including Australia (Mulley and Latter, 1980; Benzie et al., 1992, Benzie et al., 1993; Brooker et al., 2000), Thailand (Tassanakajon et al., 1997; Withyachumnarnkul et al., 1998; Klinbunga et al., 1999, Klinbunga et al., 2001; Supungul et al., 2000; Khamnamtong et al., 2009), India (Kumar et al., 2007; Mandal et al., 2012; Khedkar et al., 2013), Indonesia (Sugama et al., 2002), the Philippines (Xu et al., 2000, Xu et al., 2001), South Africa (Forbes et al., 1999) and Malaysia (Aziz et al., 2011), while the wider scale studies involved populations distributed across major continents such as eastern Africa, Southeast Asia, Australia and South Pacific islands (Bouchon et al., 1994; Duda and Palumbi, 1999; Benzie et al., 2002; You et al., 2008; Waqairatu et al., 2012). Although genetic distinctions were reported at finer to larger geographical scales, including those driven by paleo-geographical event (Waqairatu et al., 2012), all these studies except Xu et al. (2001) were conducted on shrimp individuals collected from natural populations.

In the present study, sampling coverage differs from all previous genetic studies by offering groups varying in growing environments, domesticated vs. natural populations, at a wider geographical scale using multiple molecular markers. Considering the fact that the cultured populations tend to be genetically less diverse than the wild stocks (Campton, 1995; Wolfus et al., 1997; Zhou et al., 2020), we sought to reveal two hypothesized issues in P. monodon: (i) prominence of genetic differentiation among populations of different geographical regions and (ii) possibility of discrepancy in genetic diversity levels between wild and domesticated broodstocks. Based on population genetic analyses using combined dataset of 10 microsatellite loci and mtDNA control region, this study aims to provide a useful theoretical guidance for breeding programs to produce seeds of P. monodon. Moreover, the investigation of genetic diversity status of both the wild and domesticated broodstock populations would offer to identify DNA markers potentially for using in the selective breeding, and helping to realize how domestication meditated changes in escaped farmed shrimp may impact the dynamics of wild populations.

Section snippets

Sample collection and DNA extraction

All individuals of P. monodon broodstock consisting of both domesticated and wild–caught individuals were collected from five sampling sites across Indo-Pacific regions with their sampling details as listed in Table 1. Among these five locations, P. monodon broodstock populations from MJ (Japan) and MS (Malaysia) were caught from the wild environment, while MT (Thailand), MMO (Hawaii, USA) and MD (Madagascar) were acquired from the domesticated shrimp hatcheries. After dissecting the muscle

Genetic diversity and population structure using mtDNA control region

A total of 83 mtDNA CR sequences, each with the size of 566 bp, corresponded to 80 distinct haplotypes (H), in which two MMO individuals and one MD individual shared similar haplotypes between individuals of their respective populations (Table 2). All haplotypes were divided into three clades based on haplotypes network diagram (Fig. 1). Clade C was the largest clade containing a total of 38 individuals from all five sampling sites. Haplotype 10, 42 and 45 had the largest number of shared

Discussion

This study investigated the population structure, genetic diversity and demographic history of P. monodon broodstocks collected from the natural habitats and aquaculture sites across the Indo-Pacific region using a combined panels of polymorphic microsatellite loci and mitochondrial control region sequences. Microsatellite DNA data were observed to be concordant with the mtDNA dataset in most respects. These results indicate clear genetic differentiation between the wild and domesticated

Conclusion

Besides aiming to produce high-quality seed for seafood industry, domestication of P. monodon is important for genetic improvement program, while re-establishing program using native stocks rather than mixed stocks of high genetic diversity are highly essential for the maintenance of stock diversity in the natural environment. In this study, an evident genetic divergence was observed between the wild and domesticated broodstock populations of P. monodon. Both mtDNA and microsatellite data

Abbreviations

AMOVA Analysis of molecular variance

Ar Allelic richness

CR Control region

CVA Canonical variate analysis

DNA Deoxyribose nucleic acid

FIS Fixation index

Hd Haplotype diversity

HWD Hardy-Weinberg disequilibrium

HWE Hardy-Weinberg equilibrium

IBD Isolation-by-distance

mtDNA Mitochondrial DNA

MCMC Markov Chain Monte Carlo

NJ Neighbor-joining

NRGS Niche Research Grant Scheme

PCR Polymerase chain reaction

PCA Principal component analysis

RFLP Restriction fragment length polymorphism

SSD Sum of squares deviations

WE Wahlund effect

CRediT authorship contribution statement

Conceptualization and design of the research, L.L.W. and M.A.; methodology, data collection and data analysis, L.C.C., Z.M.D., A.A.Z and L.L.W.; spatial cluster analysis, M.A., M.M.R.; writing—original draft preparation, L.L.W.; M.A. and L.C.C.; writing—review and editing, L.L.W., M.A., M.M.R., M.I. and S·I; project administration, L.L.W.; funding acquisition, L.L.W. All authors have read and agreed to the published version of the manuscript.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We would like to express our deepest gratitude to Dr. Kazutoshi Okamoto from Shizuoka Prefectural Research Institute of Fishery and Ocean, Japan for providing wild broodstocks from Japan. We would also like to thank Alunan Asli Sdn Bhd for providing domesticated broodstocks (MMO, MMD, MT) for this study.

Funding

This study was funded by Ministry of Higher Education, Malaysia under the Niche Research Grant Scheme (NRGS) (NRGS/2014/53131/6).

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