Genetic diversity analysis of brown marmorated stink bug, Halyomorpha halys based on mitochondrial COI and COII haplotypes

Abstract

Background In the past decade, the brown marmorated stink bug (BMSB), Halyomorpha halys (Hemiptera: Pentatomidae) has caused extensive damage to global agriculture. As a high-risk pest for many countries, including New Zealand, it is important to explore its genetic diversity to enhance our knowledge and devise management strategies for BMSB populations. In this study, two mitochondrial genes, Cytochrome c oxidase I (COI) and Cytochrome c oxidase II (COII) were used to explore the genetic diversity among 463 BMSB individuals collected from 12 countries. Result In total, 51 COI and 29 COII haplotypes of BMSB were found, which formed 59 combined haplotypes (5 reported and 54 novel). Of these, H1h1 was the predominant haplotype. The haplotype diversity (Hd) and nucleotide diversity (π) were high while the neutrality (Fu’s Fs) values were negative for the BMSB populations in the native countries, China, and Japan. For the BMSB populations from the invaded countries, the Fu’s Fs values were negative for populations from Chile, Georgia, Hungary, Italy, Romania, Turkey, and USA, indicating that those populations are under demographic expansion. In comparison, the Fu’s Fs values were positive for the populations from Austria, Serbia, and Slovenia, revealing a potential population bottleneck. Analysis of molecular variance (AMOVA) suggested that significant genetic difference exists among the BMSB populations from China, Japan, and the invasive countries. Conclusion This study revealed that the haplotype diversity of the BMSB populations was high in those two studied countries where BMSB is native to (China and Japan) but low in those countries which have been invaded by the species. The analysis indicated that multiple invasions of BMSB occurred in Europe and the USA. The study also revealed three ancestral lines and most of the novel haplotypes were evolved from them. Moreover, we observed two genetic clusters in the invasive populations that are formed during different invasion events. Our study provided a comprehensive overview on the global haplotypes distribution thus expanding the existing knowledge on BMSB genetic diversity that potentially could play an important role in formulating feasible pest management strategies.

Diversity and distribution of cytochrome oxidase I (COI) haplotypes of the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera, Pentatomidae), along the eastern front of its invasive range in Eurasia

“…The continued and consistent detection of one or more of these same haplotypes in Europe following the initial invasion (e.g. H1, H3, H8 and H33; Cesari et al 2015Cesari et al , 2018Gariepy et al 2015;Morrison et al 2017;Šapina and Jelaska 2018;Schuler et al 2020;Yan et al 2021), largely supports the occurrence of a bridgehead effect, wherein particularly successful invasive populations have given rise to secondary invasions in other locations (Lombaert et al 2010;Lawson Handley et al 2011). However, in Italy and Greece, subsequent introductions directly from Asia may have also taken place between 2013 and 2019, as a combined total of 20 additional haplotypes (including 14 previously undescribed haplotypes) have been reported in more recent studies in these two countries (Morrison et al 2017;Cesari et al 2018;Schuler et al 2020).…”

“…The mitochondrial Cytochrome Oxidase I (COI) gene has shown utility in species identification and separation of genetic lineages (Bucklin et al 2011;Stephens et al 2011), in particular as it relates to reconstructing routes of invasion (Auger-Rozenberg et al 2012;Chapman et al 2015). Although the Cytochrome Oxidase II (COII) gene of H. halys has also been sequenced (Xu et al 2014;Cesari et al 2015Cesari et al , 2018Yan et al 2021), the COI gene has been used more extensively in the characterisation of the invasion history, diversity and identity of H. halys haplotypes in both native and invaded regions (Gariepy et al 2014(Gariepy et al , 2015Cesari et al 2015Cesari et al , 2018Zhu et al 2016;Morrison et al 2017;Valentin et al 2017;Lee et al 2018;Horwood et al 2019;Schuler et al 2020;Yan et al 2021). Based on the COI haplotype analysis of H. halys, it has been suggested that multiple invasion events took place in the initial / early stages of invasion in Europe (2007)(2008)(2009)(2010)(2011)(2012), with the population in Switzerland (primarily haplotype H3 and H8) resulting from the establishment of individuals that arrived directly from China; the population in Italy (primarily H1) resulting from the establishment of individuals from the invasive population in the USA; and the population in Greece (predominantly haplotype H33) resulting from a separate establishment of H. halys from China (Cesari et al 2015;Gariepy et al 2015;Valentin et al 2017).…”

“…Halyomorpha halys COI haplotypes have been reported from Austria, Croatia, France, Georgia, Greece, Hungary, Italy, Romania, Serbia, Slovenia, Switzerland and Turkey (Gariepy et al 2014(Gariepy et al , 2015Cesari et al 2015Cesari et al , 2018Morrison et al 2017;Šapina and Jelaska 2018;Schuler et al 2020;Yan et al 2021). In some cases, the reports are based on a few specimens from a single location within a given country, based on their availability for study (e.g.…”

“…Identification of the haplotypes that are present in these areas may provide insight into the origin and spread of H. halys in these regions, particularly as it relates to secondary invasions from other countries in the invaded range. To address this, the DNA barcode region of the COI gene was analysed from samples collected from Georgia (including Abkhazia), Kazakhstan, Russia, Serbia and Ukraine and compared to the haplotype framework generated in previous studies (Gariepy et al 2014(Gariepy et al , 2015Cesari et al 2015Cesari et al , 2018Zhu et al 2016;Morrison et al 2017;Schuler et al 2020;Yan et al 2021). The present study builds upon a recent haplotype report from Georgia and Serbia (Yan et al 2021), but with more extensive sampling and assessment of the haplotype composition in these two countries and characterises haplotype composition from Russia, Ukraine and Kazakhstan, which have not previously been assessed.…”

“…To address this, the DNA barcode region of the COI gene was analysed from samples collected from Georgia (including Abkhazia), Kazakhstan, Russia, Serbia and Ukraine and compared to the haplotype framework generated in previous studies (Gariepy et al 2014(Gariepy et al , 2015Cesari et al 2015Cesari et al , 2018Zhu et al 2016;Morrison et al 2017;Schuler et al 2020;Yan et al 2021). The present study builds upon a recent haplotype report from Georgia and Serbia (Yan et al 2021), but with more extensive sampling and assessment of the haplotype composition in these two countries and characterises haplotype composition from Russia, Ukraine and Kazakhstan, which have not previously been assessed. Based on the characterisation of haplotypes from these areas and comparison with global records of H. halys haplotypes, we speculate on the pattern of diversity and spread and discuss the possible pathways of entry into these regions.…”