Colonization history of the western corn rootworm (Diabrotica virgifera virgifera) in North America: insights from random forest ABC using microsatellite data

Abstract

First described from western Kansas, USA, the western corn rootworm, Diabrotica virgifera virgifera, is one of the worst pests of maize. The species is generally thought to be of Mexican origin and to have incidentally followed the expansion of maize cultivation into North America thousands of years ago. However, this hypothesis has never been investigated formally. In this study, the genetic variability of samples collected throughout North America was analysed at 13 microsatellite marker loci to explore precisely the population genetic structure and colonization history of D. v. virgifera. In particular, we used up-to-date approximate Bayesian computation methods based on random forest algorithms to test a Mexican versus a central-USA origin of the species, and to compare various possible timings of colonization. This analysis provided strong evidence that the origin of D. v. virgifera was southern (Mexico, or even further south). Surprisingly, we also found that the expansion of the species north of its origin was recent-probably not before 1100 years ago-thus indicating it was not directly associated with the early history of maize expansion out of Mexico, a far more ancient event.

Resistance and Tolerance to Root Herbivory in Maize were Mediated by Domestication, Spread, and Breeding

“…Crop plants can become hosts for herbivores as a consequence of domestication, spread to new environments, and breeding for high yield, as noted previously (Chen et al, 2015a;Chen, 2016;Chen and Schoville, 2018). After maize's spread from the central Mexican highlands to North America, the oligophagous, root-chewing insect Western corn rootworm (WCR) (Diabrotica virgifera virgifera Le Conte) shifted to maize from an unknown ancestral Poeaceae host to later become a pest (Lombaert et al, 2017). WCR likely spread with maize from northern Mexico to southwestern United States (ca.…”

“…Four plant types belonging to the Zea genus were tested: Balsas teosinte, Mexican landraces, US landraces and US inbred lines (Table 1). These plant types were selected to represent the evolution of maize from its wild ancestor through the processes of domestication, spread, and breeding (Troyer, 1999;Matsuoka et al, 2002;Labate et al, 2003;Lombaert et al, 2017). Specifically, (i) Balsas teosinte is the immediate ancestor of maize, thus represented maize in its wild state, prior to domestication; (ii) Mexican landraces were included as descendants of Balsas teosinte, and served to assess the effects of domestication and the crop's early upland spread; (iii) US landraces were included as descendants of Mexican landraces, and used to assess the effects of the crop's spread to North America, and; (iv) US inbred lines were included as descendants of US landraces, and used to assess the effects of modern breeding.…”

“…Overall, our results were consistent not only with predictions concerning plant defense evolution in the contexts of plant productivity-resistance trade-offs and plant resistance-tolerance trade-offs, as noted above, but also with predictions concerning defense strategy evolution in the context of variable resource availability and environmental stresses, particularly physiological stress (under low resource availability) and herbivory pressure (Herms and Mattson, 1992;Blossey and Notzold, 1995;Zou et al, 2007;Hahn and Maron, 2016) (Figure 8). We believe that shifts in resource availability, WCR pressure, and farmer selection of maize landraces to systematic breeding of maize inbred lines between the pre-intensification and intensification periods of maize production mediated the evolution of WCR defenses in US inbred maize lines (Duvick, 2005;Gray et al, 2009;Ivezić et al, 2009;Kutka, 2011;Smith, 2011;Lombaert et al, 2017;Mesa et al, 2017). For example, while the slight gain in WCR resistance evident in US inbred lines was not anticipated per expectations under a productivity-resistance trade-off, it was an anticipated result of directed systematic breeding for WCR resistance (and inadvertent selection under WCR pressure), and was associated with a loss of tolerance, as anticipated under a resistance-tolerance trade-off (Duvick, 2005;Agrawal, 2006;Agrawal and Fishbein, 2008;Gray et al, 2009;Ivezić et al, 2009;Agrawal et al, 2010).…”

Potential global distribution of Diabrotica species and the risks for agricultural production

“…The western corn rootworm is native to Mexico and incidentally followed the expansion of maize cultivation into North America thousands of years ago. 54 More recently, the species was introduced in Europe and has continued to spread to several countries within central continental Europe. In its native and invaded range, D. v. virgifera occurs in regions with semi-arid, subtropical, and humid continental climates.…”

Comparative analysis of adaptive and neutral markers ofDrosophila mediopunctatapopulations dispersed among forest fragments

“…Microsatellite loci are codominant multi-allelic genetic markers, which allow assessing both temporal and spatial genetic structure of natural populations (Gredler, Hish, & Noor, 2015;Hartvig et al, 2018;Silva, Machado, & Mateus, 2015). They are also a marker commonly used in conservation genetics to estimate the loss of genetic variability and to infer the demographic history of populations, assuming they are neutral or nearly neutral even if located in a coding region (Ellegren, 2004;Lombaert et al, 2018;Stamenković-Radak et al, 2012;Takezaki, 2017).…”