Genetics of lineage diversification and the evolution of host usage in the economically important wheat curl mite, Aceria tosichella Keifer, 1969

Abstract

BackgroundUnderstanding the mechanisms that underlie the diversification of herbivores through interactions with their hosts is important for their diversity assessment and identification of expansion events, particularly in a human-altered world where evolutionary processes can be exacerbated. We studied patterns of host usage and genetic structure in the wheat curl mite complex (WCM), Aceria tosichella, a major pest of the world’s grain industry, to identify the factors behind its extensive diversification.ResultsWe expanded on previous phylogenetic research, demonstrating deep lineage diversification within the taxon, a complex of distinctive host specialist and generalist lineages more diverse than previously assumed. Time-calibrated phylogenetic reconstruction inferred from mitochondrial DNA sequence data suggests that lineage diversification pre-dates the influence of agricultural practices, and lineages started to radiate in the mid Miocene when major radiations of C4 grasses is known to have occurred. Furthermore, we demonstrated that host specificity is not phylogenetically constrained, while host generalization appears to be a more derived trait coinciding with the expansion of the world’s grasslands. Demographic history of specialist lineages have been more stable when compared to generalists, and their expansion pre-dated all generalist lineages. The lack of host-associated genetic structure of generalists indicates gene flow between mite populations from different hosts.ConclusionsOur analyses demonstrated that WCM is an unexpectedly diverse complex of genetic lineages and its differentiation is likely associated with the time of diversification and expansion of its hosts. Signatures of demographic histories and expansion of generalists are consistent with the observed proliferation of the globally most common lineages. The apparent lack of constrains on host use, coupled with a high colonization potential, hinders mite management, which may be further compromised by host range expansion. This study provides a significant contribution to the growing literature on host-association and diversification in herbivorous invertebrates.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1234-x) contains supplementary material, which is available to authorized users.

Reactive oxygen species metabolism and photosynthetic performance in leaves of Hordeum vulgare plants co-infested with Heterodera filipjevi and Aceria tosichella

“…This is the most significant economic impact of WCM on cereal yielding. As a result of WCM feeding or WSMV transmission on cereal leaves, the grain yield losses may reach up to 40% (Skoracka et al 2017(Skoracka et al , 2018aAguirre-Rojas et al 2019).…”

Genome Size Reversely Correlates With Host Plant Range in Helicoverpa Species

“…Speciation often leads to expansion or contraction in genome size and host range (Moran, 2002; Parkhill et al, 2003; Cho et al, 2007; Thomson et al, 2008; Merhej et al, 2013; Langridge et al, 2015; Skoracka et al, 2018). Organisms may expand their host range by adapting to different host environments via evolving additional host use related metabolic pathways and genes involved in digestion and detoxification, or by modifying distinct host environments to one or a few standard nutrient environments to which they are specialized via secretion of effectors, toxins and host-cell interaction proteins (Parkhill et al, 2003; Thomson et al, 2008; Boothroyd, 2009; McNally et al, 2014; Langridge et al, 2015; Baroncelli et al, 2016).…”

Temperature-dependent development and survival of an invasive genotype of wheat curl mite, Aceria tosichella

“…The accumulation of basic biological data represents an essential resource for comprehensive studies of species like wheat curl mite. In addition to being an economically important pest species, WCM is the de facto model for the study of Eriophyoidea, due to the relative ease with which it can be collected from the field, on at least four continents (Carew et al 2009;Skoracka et al 2012Skoracka et al , 2014bSkoracka et al , 2018aMiller et al 2013;Karpicka-Ignatowska et al 2019;Khalaf et al 2020), and with which it can be cultured in the laboratory (e.g., Karpicka-Ignatowska et al 2019), as well as its well-documented genetic and physiological diversity (Carew et al 2009;Hein et al 2012;Navia et al 2013;Szydło et al 2015; 6.9 6.5-7.5 29 6.7 6.2-7.2 30 6.4 5.9-6.9 31 6.2 5.6-6.8 32 5.9 5.3-6.7 33 5.7 5.0-6.6 Skoracka et al 2018a). Such studies have yielded important data on passive dispersal in microscopic eukaryotes (Laska et al 2019;Karpicka-Ignatowska et al 2019), virus transmission by herbivorous arthropods (Seifers et al 2002;Schiffer et al 2009;Navia et al 2013;Hein 2015, 2017;Wosula et al 2018;Singh et al 2018;Tatineni and Hein 2018), physiology (Wosula et al 2015), genetics (Miller et al 2013;Skoracka et al 2018a), ecology and behavior (Kiedrowicz et al 2017;Laska et al 2019), distribution (Schiffer et al 2009;Navia et al 2010Navia et al , 2013Skoracka et al 2014b;Khalaf et al 2020), as well as specific assessments of its impact on crop losses (Navia et al 2013;…”