Population genetics of the brown marmorated stink bug Halyomorpha halys in the early phase of invasion in South Tyrol (Northern Italy)

Abstract

The brown marmorated stink bug Halyomorpha halys is one of the most harmful invasive species in the world. Native to East Asia, this insect was introduced into North America in the 1990s and into Europe in the 2000s where it subsequently established and spread across the continent. Previous population genetic studies determined the invasion pathways at continental and national levels. However, information on the dynamics on a small-scale is currently scarce. Here we study the genetic diversity and population dynamics of H. halys in South Tyrol, a region in Northern Italy, since its arrival to its widespread establishment over a period of four years. By haplotyping 162 individuals from ten populations (including six previously published individuals) we found a high haplotype diversity in most populations with an increasing diversity across the different years. Most haplotypes were previously found in other regions of Northern Italy, providing evidence for migration from neighboring regions. However, the presence of four previously undescribed haplotypes as well as a haplotype previously found exclusively in Greece highlights additional long-distance dispersal across the continent. Phylogenetic analysis of the haplotypes found in South Tyrol showed that the majority of haplotypes clustered with haplotypes predominantly found in Japan. This suggests a potential recent introduction of H. halys individuals from Japan into Europe, and thus an additional invasion pathway that was previously unidentified.

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).…”

“…Additionally, based on current data and previous publications (e.g. Gariepy et al 2014Gariepy et al , 2015Cesari et al 2015Cesari et al , 2018Šapina and Jelaska et al 2018;Schuler et al 2020;Yan et al 2021), the number of COI haplotypes and the identity of dominant haplotypes from invaded European and central Asian countries were tallied and used to generate an overview of the trends and dominant haplotypes in these areas.…”

“…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.…”