Species delimitation and invasion history of the balsam woolly adelgid, Adelges (Dreyfusia) piceae (Hemiptera: Aphidoidea: Adelgidae), species complex

Abstract

The Adelges (Dreyfusia) piceae (Ratzeburg) species complex is a taxonomically unstable group of six species. Three of the species are cyclically parthenogenetic [Ad. nordmannianae (Eckstein), Ad. prelli (Grossmann), and Ad. merkeri (Eichhorn)] and three are obligately asexual [Ad. piceae, Ad. schneideri (Börner), and Ad. nebrodensis (Binazzi & Covassi)]. Some species are high‐impact pests of fir (Abies) trees, so stable species names are needed to communicate effectively about management. Therefore, to refine species delimitation, guided by a reconstruction of their biogeographic history, we genotyped adelgids from Europe, North America, and the Caucasus Mountains region with 19 microsatellite loci, sequenced the COI DNA barcoding region, and compared morphology. Discriminant analysis of principal components of microsatellite genotypes revealed four distinct genetic clusters. Two clusters were morphologically consistent with Ad. nordmannianae. One of these clusters consisted of samples from the Caucasus Mountains and northern Turkey, and the other included samples from this region as well as from Europe and North America, where Ad. nordmannianae is invasive. A third cluster was morphologically consistent with Ad. piceae, and included individuals from Europe, where it is native, and North America, where it is invasive. In North America, the majority of Ad. piceae individuals were assigned to two geographically widespread clones, suggesting multiple introductions. The fourth cluster included individuals morphologically consistent with Ad. prelli or Ad. merkeri. However, based on genetic assignments, hybrid simulations, and approximate Bayesian computation, we find it likely that these are contemporary hybrids between Ad. nordmannianae and Ad. piceae that arose independently in Europe and North America, so we propose that Ad. prelli and Ad. merkeri are invalid. Finally, we synonymise Ad. schneideri (syn.n.) with Ad. nordmannianae and designate Ad. nebrodensis as subspecies Ad. piceae nebrodensis (stat.n.). Our revised taxonomy therefore recognises two species: Ad. nordmannianae and Ad. piceae, which we estimate to have diverged recently, during one of the last two interglacial periods. Finally, we comment on this species complex being in the midst of transition between sexual and asexual reproduction, a pattern that is probably common in Adelgidae.

Mitogenomes provide new insights of evolutionary history of Boreheptagyiini and Diamesini (Diptera: Chironomidae: Diamesinae)

“…The evolutionary rate analyses of Diamesinae also provided new insights for the study of species delimitation. The evolutionary rate of COI was generally considered to be consistent with the evolutionary rate of the species itself, so it has been widely used in species delimitation and phylogenetic studies (Havill et al, 2021 ; Jones et al, 2021 ). However, for species with lower evolution rate of mitochondrial PCGs, COI barcodes sometimes failed to accurately define the species boundary of Diamesa (Montagna et al, 2016 ) (E. Stur, pers.…”

Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae)

“…During periods of relaxed selection, when adelgids feed on nutrient-rich galls on spruce hosts, accelerated gene inactivations in the nutrient-provisioning pathways should occur indiscriminately between these dual symbionts, allowing either symbiont to reduce its nutrient-provisioning responsibilities or to acquire a partnership-ending mutation. Periods of increased selection, when adelgids feed on nutrient-poor phloem of alternate hosts, can occur yearly for populations that regularly alternate between spruce and other conifers, or can last for up to thousands of years for populations on alternate hosts separated from spruces due to glacial cycles or invasions to new environments [ 36 , 106 ]. Thus, the varied nutrient provisioning contributions of adelgid symbionts may be a consequence of historical and contemporary fluctuations in host dietary quality that spurs symbiont genome decay and turnover [ 15 , 28 ].…”

Weak spatial-genetic structure in a native invasive, the southern pine beetle (Dendroctonus frontalis), across the eastern United States

“…Dataset abbreviations are as follows: augmented dataset (ADS; 33 loci), low noise dataset (LNDS; 24 loci), high sensitivity datasets (HSDS; either 10 or 19 loci), males and females (m+f), males only (m), and females only (f). into newly invaded areas, and provide insights into the relative importance of natural vs. human-mediated dispersal (e.g., fire ants, Ascunce et al, 2011;termites, Perdereau et al, 2013;hemlock woolly adelgid, Havill et al, 2016;Havill et al 2021). These inferences have implications for management, such as enabling targeted control (e.g., of an invasive ''bridgehead'' population that is the primary source of subsequent spread (Lombaert et al, 2010) and which may have evolved higher invasiveness (Whitney & Gabler, 2008), or enhanced surveillance of ''stowaways'' where transportation networks are involved in accelerating spread (e.g., via inadvertent movement of contaminated live plants, wood packing materials, or firewood; Meurisse et al, 2019).…”

“…Spatially explicit population genetic analyses of microsatellite data from invasive insect species can identify the geographic origin(s) and number of independent introductions into newly invaded areas, and provide insights into the relative importance of natural vs. human-mediated dispersal ( e.g. , fire ants, Ascunce et al, 2011 ; termites, Perdereau et al, 2013 ; hemlock woolly adelgid, Havill et al, 2016 ; Havill et al 2021 ). These inferences have implications for management, such as enabling targeted control ( e.g.…”