Genetic homogeneity detectable in the sedentary moray eel Gymnothorax minor based on mitochondrial DNA analysis

https://doi.org/10.1016/j.rsma.2020.101504Get rights and content

Highlights

  • G. minor populations in coastal China displayed very high genetic diversity.

  • PLD promoted gene exchange between panmictic populations of G. minor in coastal China.

  • Distant leptocephalus transfer by ocean currents shrank geographic-genetic structure.

Abstract

On the basis of traditional morphological classification, Gymnothorax minor has been misidentified as Gymnothorax reticularis in China. Because of the special ecological habits and aggressiveness of this species, little research has been performed on its population genetics. Given the general decline in offshore fishery resources, it is necessary to study the genetic characteristics of G. minor in order to protect this resource. In the present study, six different geographical populations of G. minor were collected from their distribution areas in China, and their genetic signatures were investigated for the first time based on the control region fragments. The results showed that G. minor had a very high degree of genetic diversity, and there was no genetic differentiation between these populations. However, the genetic analysis failed to reject panmixia among geographic populations of this species. The life-history characteristics of G. minor and the heterogeneity of its habitat promote the rapid growth of its populations, resulting in gene mutation accumulation and rich genetic diversity. G. minor experienced a population expansion event during the late Pleistocene, which shaped its various genetic signatures. The prolonged pelagic larval duration (PLD) of this species ensures that its leptocephali effectively avoid various physical obstacles and have the opportunity to follow ocean currents to various coastal areas of China. Finally, this moray eel exchanges genetic material with recruitment populations from other locations. All the current genetic signature results for G. minor will serve as a reference for genetic research on moray eels with similar life-history characteristics.

Introduction

In open seas that lack obvious physical obstacles, marine organisms can engage in free gene flow in most situations and will not undergo genetic differentiation. However, in species that are characterized by weakly mobile adults, are nonmigratory, exhibit natal homing characteristics, and produce pelagic larvae, genetic structure is more complicated and is affected by various biological and environmental factors. These factors are difficult to parameterize (Huang et al., 2018). For fishes with such characteristics, pelagic larval duration (PLD) is often used as an important indicator to study their population connectivity and genetic signatures (Reece et al., 2010, Huang et al., 2018). Larval fishes use different external habitats during their early life and display different life-history characteristics, which result in a PLD specific to each population (Bay et al., 2006).

Moray eels, belonging to Anguilliformes, are a speciose lineage. Most moray eels inhabit rocky ledges and coral reefs from the intertidal zone to depths of over 300 m (Tsukamoto et al., 2014), have high fidelity to their habitats (Bassett and Montgomery, 2011), and spawn without migrating (Moyer and Zaiser 1982). They are abundant in coral reef ecosystems. Moray eels are the main mesopredators in coral reef ecosystems and thus play a vital role in the food webs of these ecosystems. It is difficult to collect biological samples of anguilliform species because they are nocturnal and aggressive. Therefore, little attention has been paid to their population genetics.

All moray eels have a relatively long leptocephalus larval stage, but most of their spawning activity is unclear (Kimura et al., 2004). A long PLD gives coral reef fishes whose adults are sedentary the ability to float long distances with ocean currents and choose suitable habitats, thereby expanding their population distribution and facilitating genetic material exchange. Therefore, coral reef fishes with a long PLD likely have strong potential for gene flow and little genetic structure, a pattern that has been observed in some coral reef fishes (Reece et al., 2010, Huang et al., 2018, Ribout et al., 2018). However, some other coral reef species do not conform to this hypothesis, instead exhibiting significant genetic structure between different populations (Planes and Fauvelot, 2002, Swearer et al., 2002). Therefore, although some coral reef fishes (especially those with a long PLD) have similar life histories, their final genetic structures and structure-forming mechanisms may be different. These results have motivated marine biologists to study ocean currents, life-history characteristics, habitat preferences, fixation mechanisms, and responses to climate change.

Gymnothorax minor (Temminck & Schlegel, 1846) is a typical coral reef fish. It has been misidentified as Gymnothorax reticularis Bloch, 1795 in China (Li et al., 2018a, Li et al., 2018b). Although the yield of G. minor is not high, this fish has moderate economic value. The life-history characteristics and genetic signatures of G. minor are still unknown. It is unclear whether this species has a long PLD before settlement, as observed in most moray eels, and whether the leptocephali randomly drift with currents and thus cause genetic mixing. It is also unclear whether G. minor forms specific genetic structure due to its habitat preferences, natal homing, and canalized propagule dispersal. We believe that some of these uncertainties can be addressed by using molecular genetic markers. The molecular markers used in early spatiotemporal-scale molecular genetic studies of moray eels mainly included the mitochondrial Cytb and COI genes and nuclear genomic markers, namely, RAG-1 gene, RAG-2 gene, and simple sequence repeat (SSR) markers (Kimura et al., 2004, Reece et al., 2010, Huang et al., 2018, Ribout et al., 2018).

The present study examined, for the first time, the genetic signatures of G. minor at a relatively fine spatial scale, based on the first hypervariable region of the control region (CR) of mitochondrial DNA, and elucidated the genetic diversity, genetic structure, and historical dynamics of this species. Our findings reveal the effects of paleoclimate, paleogeological events, the marine geological environment, and other factors on the population formation, distribution and diffusion pathways, and gene exchange of G. minor. In addition, the present study explored the mechanism leading to the current systematic geographic pattern of this species. With the general decline in fishery resources, G. minor resources have inevitably declined. Therefore, it is necessary to understand the genetic characteristics of G. minor populations, including their genetic diversity, genetic structure, and effective population size, which are required to formulate strategies for the effective protection and rational development and utilization of marine fishery resources (Funk et al., 2012).

Section snippets

Sample collection

From March to November 2019, a total of 136 individuals of G. minor were collected successively in six coastal areas of China where the species is frequently observed: Xiamen (XM), Dongshan (DS), Lufeng (LF), Yangjiang (YJ), Lingshui (LS), and Wenchang (WC) (Fig. 1, Table 1). To ensure sample accuracy, all individuals were subjected to species identification based on their external morphological characteristics (Nakabo, 2013, Yamada et al., 2009). The dorsal muscles were excised from all

Genetic diversity

All sequences were subjected to manual alignment and correction. As a result, 136 target fragments were obtained, which were 579–580 bp in length. Among these fragments, only three had a length of 579 bp; thus, 580-bp sequences were by far the most common. There were 116 variable sites, 88 parsimony-informative sites, 28 singly informative sites, and three insertion/deletion sites. The ratio of transition to transversion was 4.19, indicating that the target fragments had not reached a state of

Discussion

This species G. minor is nocturnal and exhibits a certain degree of aggressiveness. Therefore, specimen collection is somewhat difficult, explaining the lack of studies on the population genetics of this species. We examined the genetic signatures of G. minor for the first time, using mitochondrial CR fragments to reflect the true genetic diversity level and the current genetic structure of this species. Six geographical populations of G. minor were collected from north to south along the coast

Conclusion

In the past, G. minor was misidentified as G. reticularis in China, and related research was limited to species identification. G. minor has a moderate yield and economic value in China. However, research on the resource status and genetic diversity level of G. minor is lacking. The present study showed that, similar to other moray eels, G. minor displays a very high degree of genetic diversity. There is no genetic differentiation between geographic populations, but there is frequent genetic

CRediT authorship contribution statement

Yuan Li: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft, Writing - review & editing. Liyan Zhang: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft, Writing - review & editing. Puqing Song: Data curation, Formal analysis, Software. Binbin Shan: Investigation, Methodology, Supervision. Longshan Lin:

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

The present study could not have been performed without assistance from Mr. Yanping Wang and Haozhan Wang during the collection of G. minor specimens. We also thank the anonymous reviewers for their helpful comments. This work was supported by the Natural Science Foundation of Fujian Province, China [grant number 2019J05146]; the National Programme on Global Change and Air-Sea Interaction, China [grant numbers GASI-02-SCS-YDsum/spr/aut], the Bilateral Cooperation of Maritime Affairs, China

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    The authors contributed equally to this paper.

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