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

Abstract

The arrival, establishment and pest status of Halyomorpha halys in Europe and non-native countries in Asia have been well-documented, with thorough characterisation of the genetic diversity and occurrence of cytochrome oxidase I (COI) haplotypes in Switzerland, France, Hungary, Italy and Greece. However, a number of gaps exist in terms of the characterisation of the haplotype diversity and occurrence of H. halys along the invasion front that covers eastern Europe, western and central Asia. To contribute towards filling this gap, the COI haplotype diversity and distribution were investigated for H. halys collected in Serbia, Ukraine, Russia, Georgia and Kazakhstan. A total of 646 specimens were analysed and five haplotypes were found (H1, H3, H8, H33 and H80). Haplotype H1 was present in all five countries investigated and was the only haplotype detected amongst > 500 specimens collected from Ukraine, Russia and Georgia. H1 (82%) was the dominant haplotype found in Kazakhstan, alongside H3 (18%). In contrast to the low or no diversity observed in these four countries, Serbia had higher haplotype diversity and was represented by five haplotypes. Although H3 was dominant (47%) in Serbia, H1 was also prevalent (40%); the remaining haplotypes (H8, H33 and H80) were minor contributors (1–11%) to the haplotype composition. The results are discussed in context with other known populations in neighbouring countries and patterns of haplotype diversity indicate the movement of successful invasive populations in Europe to generate secondary invasions along the eastern front of the invasion in Eurasia. Possible scenarios regarding the spread of particular haplotypes in these regions are discussed, along with suggestions for future research to fill existing gaps.

First record of the invasive true bug (Heteroptera) Halyomorpha halys (Stål, 1855) from Hamburg with other records from Northern Germany and possible implications for its range expansion

“…The sequence was deposited in NCBI Genbank under accession MZ828400. It represents the haplotype H3 from Yan et al ( 2021) and Gariepy et al (2021) and matched other sequences of H. halys in BOLD and GenBank with 100%; several sequences (specimens from Serbia, Hungary, China, Austria and Italy) clustered with it (Fig. 2).…”

Flying over Eurasia: Geographic Variation of Photoperiodic Control of Nymphal Development and Adult Diapause Induction in Native and Invasive Populations of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae)

“…It should be noted, however, that South Korea is a part of the native geographic range of H. halys , whereas the other populations represent the invasive range [ 20 , 21 , 22 , 23 , 25 ].…”

“…Among the most invasive insects is the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae), which originates in eastern Asia (China, Korea, Japan, Myanmar, Vietnam, and Taiwan). It is now considered one of the most harmful invasive insect pests in North America and Europe [ 20 , 21 , 22 , 23 , 24 ] and was also recently recorded in Russia [ 24 , 25 , 26 ]. Native and invasive ranges remain disconnected in Eurasia with a lower diversity of haplotypes in Europe than in Asia [ 22 ].…”

“…It is now considered one of the most harmful invasive insect pests in North America and Europe [ 20 , 21 , 22 , 23 , 24 ] and was also recently recorded in Russia [ 24 , 25 , 26 ]. Native and invasive ranges remain disconnected in Eurasia with a lower diversity of haplotypes in Europe than in Asia [ 22 ]. Halyomorpha halys overwinters as an adult and its reproductive diapause is induced by short photoperiods.…”

Biological Parameters, Phenology and Temperature Requirements of Halyomorpha halys (Hemiptera: Pentatomidae) in the Sub-Mediterranean Climate of Western Slovenia

“…Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae), also known as the brown marmorated stink bug, is native to East Asia and has rapidly become a globally distributed invasive species by stowing away on traded goods and people traveling [ 1 ]. Accidental multiple introductions and spread of H. halys outside its native range were first reported in North America [ 2 , 3 ] and central–southern Europe [ 4 , 5 ] followed by the subsequent invasion in Eurasia [ 6 ], South America [ 7 ] and North Africa [ 8 ]. This polyphagous pest with an extremely wide host range [ 9 ] has a high capacity to cause damage to agricultural production.…”