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Population genetic structure of Bactrocera dorsalis based on cox1 sequences from Bangladesh and neighboring countries

https://doi.org/10.1016/j.aspen.2021.02.011Get rights and content

Highlights

  • High gene flow was found among all the populations, except 4 locations.

  • The colonization process can be seen as a progressive to rapid expansion.

  • The sudden expansion of populations was found in BDJ and BDR region of Bangladesh.

  • B. dorsalis could be the main insect pest of fruit crops in Bangladesh.

Abstract

Oriental fruit fly, Bactrocera dorsalis (Hendel), is a destructive and highly polyphagous invasive fruit fly species of numerous fruit crops in global agriculture. Population genetic structure of this species from five different locations of Bangladesh was examined with other samples (collected from GenBank) from 15 sites of neighboring Asian countries. A fragment of 770 bp mitochondrial DNA cox1 was used to investigate the genetic diversity and the relationship between genetic patterns and geographical distribution of B. dorsalis. A total of 232 variable sites (33.23% of the 698 bp aligned consensus sequences) and 419 unique haplotypes were identified from 710 individuals. Indices of genetic diversity suggested that without exclusion from geographical areas, B. dorsalis retained a relatively high degree of genetic diversity. A demographic assessment [Tajimas’ D test, Fu’s Fs test and sum of square deviation (SSD values)] revealed that both current and historical variables performed a significant role in deciding the weak genetic structure with some exceptions. In Bangladesh, high levels of genetic diversity with a weak genetic structure indicated that the severity of this pest might increase in the future. Proper management techniques should be taken to overcome the future severity of this kind of destructive insect.

Introduction

Tephritids are a group of agricultural pests that damage a wide range of fruits and vegetables and posing tremendous threats worldwide, with both quantitative and qualitative losses (FAO/IAEA, 2013). In the world, about 4000 described species from 500 genera of tephritids were identified (Qin et al., 2015). Among them, >250 species are considered economically important (Li et al., 2013). Most of them are belonging to six genera: Bactrocera, Ceratitis, Anastrepha, Dacus, Zeugodacus, and Rhagoletis (White and Elson-Harris, 1992, Van Houdt et al., 2010). Moreover, 118 species have been known to occur on the Indian subcontinent as cultivation fruits and vegetable pests (David and Ramani, 2011, Drew and Romig, 2013, David et al., 2016). In Bangladesh, fruit flies also cause massive damage to both vegetables and fruit production (Leblanc et al., 2018). Recently, 29 fruit fly species (13 pests and 16 non-pest species) had been identified from the rural environment and forest areas of Bangladesh by six years’ surveys (2013–2018), of which Bactrocera dorsalis (Hendel), Bactrocera zonata (Saunders), Zeugodacus tau (Walker) and Zeugodacus cucurbitae (Coquillett) were defined as major species (Alim et al., 2012).

Bactrocera dorsalis (Hendel) known as the oriental fruit fly, is a devastating agricultural pest of a large number of tropical and subtropical fruits (Leblanc et al., 2019). The possible introduction to new fruit growing area of this species is a worldwide severe concern. Due to its high invasiveness and strong adaptability to the new environment, it is considered one of the most economically important pests (Leblanc et al., 2013). In many literatures it has been reported that B. dorsalis was documented from Taiwan, China in 1911 for the first time, and it spread throughout Asia (including many other provinces in China) and several Pacific regions (Drew and Raghu, 2002; Choudhary et al., 2014). But recently, Clarke et al. (2019) reported that B. dorsalis was first recorded in “East India” (India orientali) under the synonymous name of Musca ferruginea. In Bangladesh, B. dorsalis is also known as a major agricultural pest, and its recorded main hosts are mango (Mangifera indica), carambola (Averrhoa carambola), and guava (Psidium guajava) (Kabir et al., 1991, Drew and Raghu, 2002, Huque, 2006).

The genetic structure and diversity are essential elements for studying the population genetic structure of insect species. Comparative studies can thus enable us to understand the factors affecting their population level. A set of individual or combined factors, including climate change, environmental and biological barriers, human activities, migration, natural barriers, and gene flow, can affect each species' genetic diversity and population structure (Nater et al., 2013).

Genome sequences can be exploited for the development of tools for the origin and population dynamics of invasive species (Aketarawong et al., 2014). With regard to phylogeography, mitochondrial DNA (mtDNA) is a ubiquitous and robust evolutionary marker for Intra- and interspecific relations due to characteristics such as no recombinant, large numbers of copies, lower effective population size, rapid rates of evolution, and simple maternal heritage (Kabir et al., 1991, Wan et al., 2011, Nardi et al., 2005, Prabhakar et al., 2012a, Prabhakar et al., 2012b). In particular, the mitochondrial DNA is insightful to re-build historical processes, such as deciding the species' area of origin, invasion paths, spreading and historical populations of alien species (Bryja et al., 2010, Rollins et al., 2011).

Till now to study the population genetics of B. dorsalis, most of the researchers used cytochrome c oxidase subunit I (COI) gene sequences (Roderick and Navajas, 2003). Though Wolbachia, can affect the genetic diversity (Turelli et al., 1992) but the infestation rate is very low in Bactrocera dorsalis (Sun et al., 2007, Gichuhi et al., 2019). Consequently, information on genetic variation, population structure, and gene flow patterns are therefore useful in a broad effort to control insect pests (Krafsur, 2005).

Population genetic structure has been studied in global or in specific areas from several Tephritidae species. Up to now, demographic history and population genetic structure of B. dorsalis were studied from Chinese, Southeast Asian and Indian populations (Wan et al., 2011, Aketarawong et al., 2007, Li et al., 2007, Li et al., 2009, Li et al., 2012, Choudhary et al., 2016) as well as the global (Qin et al., 2018). The genetic diversity and genetic variation of B. dorsalis in the Chongqing region of China were investigated by Wan et al. (2011). Findings indicated that the mountains in this area were not high enough to deter long-distance migration of this species and suggested a high level of gene flow among fly species. Nevertheless, Li et al. (2012) found that B. dorsalis spread was slowed down by spatial distance from the mountains and canyons scattered through China, Vietnam, and Thailand, suggesting the genetic differentiation between these areas. Individual invasions from Southern Asia led to occurrences in Africa and Hawaii, though Southern Asia (India and Bangladesh) is also possibly an origin of other Asian populations (Qin et al., 2018). But no detailed studies have yet been reported among the Bangladeshi populations. In this study, we investigated the genetic structure and genetic diversity of B. dorsalis in five different locations of Bangladeshcompared it with the other 15 sites of six Asian countries through molecular variations of a fragment of mtDNA cox1 gene.

Section snippets

Samples information

Adult B. dorsalis populations were collected from 5 different geographic locations of Bangladesh during 2017–2018. Methyl Eugenol (ME) type lure was used for trapping adult fruit flies from the commercial vegetable garden, commercial mango orchard, and guava orchard. The collected specimens were identified on the basis of morphological features (Choudhary et al., 2014; Drew and Raghu, 2002) and preserved (100% ethanol at −20 °C) prior to the extraction of DNA. Other sequences of 15 sites from

Nucleotide information and Intra-population diversity

Seven hundred ten sequences (125 from Bangladeshi samples and others were collected from GenBank) of B. dorsalis were aligned together for population genetic study from 20 sites of Bangladesh and some other Asian countries. Finally, 698 bp sequences length containing 66.3% of A + T (30.8% A and 35.5% T) and 33.7% G + C (14.8% G and 18.9% C) were used for analysis. Out of 698 nucleotide positions, 232 variable (polymorphic) sites (33.23% of the 698 bp alignment), including 162 parsimony

Median joining (MJ) network among haplotypes

The MJ network for five Bangladesh populations (BDD, BDR, BDB, BDK, BDJ, BD) of B. dorsalis were presented in Fig. 3A. Results showed that haplotypes at higher frequency (e.g., H1, H4, H11, H18, H45, H54) were located centrally and connected to rare haplotypes through few mutations. Three haplotypes (e.g., H5, H39, H40) shared with one population. The most frequent haplotypes H1 shared by three populations except BDJ and BDR population.

The MJ network for all 20 populations (Fig. 3B) was divided

Discussion

The mtDNA cox1 sequence analysis showed that genetic diversity of B. dorsalis was strongly exemplified by the high Hd, K and P values in cox1 gene analyses (Table 2). The sample size did not influence the haplotypes diversity (Hd), the average number of nucleotide differences (K) and nucleotide diversity (P), suggesting there were acceptable genetic diversity indices for the populations of B. dorsalis (Choudhary et al., 2016). The analyzed populations are stable and have a long evolutionary

Conclusion

The population genetic structure of B. dorsalis in five different locations of Bangladesh was studied and also made the comparison with the other 15 sites of Asian countries (collected from GenBank). We provide evidence on the basis of Cox 1 gene sequence that there is high gene flow among most the south Asian countries, except for two locations of western part of Bangladesh (BDJ and BDR), Myanmar and Yunnan province of China. From this study, it can be hypothesized that the central part of

Author contribution

Z.L., S.A., and M.S.N designed the study. S.A., M.S.N, and S.M.K.C collected the samples. S.A. and M.S.N extracted the DNA. S.A., M.S.N, Y.Z., Y.Q. and Z.L. assembled and analyzed the DNA sequences. S.A. and M.S.N wrote the first version of the manuscript. Z.L., Y.Z. and Y.Q. revised and modified the manuscript. All of the authors read and approved the final version of the manuscript.

Funding

This work was supported by the Natural Science Foundation Project of China (No. 31972341).

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 thank to Mr. Yousuf (Sublime Agro Ltd. Dhaka, Bangladesh) and Mr. Ehasan Ullah (Lecturer, Govt. Shahid Akbar Ali Science and Technology College, Takurgan, Bangladesh), helped us during the samples collection from Bangladesh. We also thank to the other Plant Quarantine and Invasion Biology Laboratory members, China Agricultural University (CAUPQL).

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