Cropland connectivity affects genetic divergence of Colorado potato beetle along an invasion front

Abstract

The population genetic structure of invasive species can be strongly affected by environmental and landscape barriers to dispersal. Disentangling the relative contributions of these factors to genetic divergence among invading populations is a fundamental goal of landscape genetics with important implications for invasion management. Here, we relate patterns of genetic divergence in a global invasive agricultural pest, Colorado potato beetle (CPB; Leptinotarsa decemlineata), to environmental and landscape factors along an invasion front in Northwestern China. We first used microsatellite markers and spatial‐temporal samples to assess broad patterns of genetic diversity as well as fine‐scale changes in patterns of genetic divergence. We then distinguished the relative contributions of five factors to genetic divergence among front populations: geographic distance (isolation by distance), climate dissimilarity (isolation by environment), and least‐cost distances (isolation by resistance) modeled with three factors: climate suitability, cropland cover, and road networks. Genetic diversity broadly decreased from West to East, with the exception being Eastern China. Low levels of genetic diversity and varying degrees of divergence were observed in Northwestern China, reflecting the potential effect of landscape heterogeneity. Least‐cost distance across cropland cover was most positively correlated with genetic divergence, suggesting a role of croplands in facilitating gene flow. The contribution of climate to genetic divergence was secondary, whether modeled in terms of local adaptability or connectivity of the climatic landscape, suggesting that constraints to CPB gene flow imposed by a harsh climate may be ameliorated in agricultural landscapes. No evidence was found for an obvious effect of road networks on genetic divergence and population structuring. Our study provides an example of how agricultural landscape connectivity can facilitate the spread of invasive pests, even across a broad climatic gradient. More broadly, our findings can guide decisions about future land management for mitigating further spread.

Polygenic adaptation contributes to the invasive success of the Colorado potato beetle

“…In addition, our demographic history analysis revealed a sharp decline in effective population size occurring across populations ~200 generations ago, reflecting a single bottleneck in the shared history of these populations that is consistent with records of the initial introduction to Europe (de Wilde & Hsiao, 1981), assuming an average of two generations per year (Popova, 2014). This, combined with evidence from previous studies using microsatellites, mitochondrial haplotypes and amplified fragment length polymorphism markers (Grapputo et al, 2005;Yang et al, 2021), suggests that CPB experienced strong population bottlenecks following the invasion of Eurasia, despite anecdotal evidence of multiple potential invasion events (Hurst, 1975;Lockwood, 2012).…”

Ring distribution patterns—diversification or speciation? Comparative phylogeography of two small mammals in the mountains surrounding the Sichuan Basin

“…IBE implies that genetic divergence increases with environmental heterogeneity (Wang & Bradburd, 2014). We used three complementary statistical methods that are widely used to investigate the correlation between genotypes and geographical and environmental components (Forester et al, 2018; Huang et al, 2016; Kierepka & Latch, 2015; Wang, 2013; Yang et al, 2020), namely the Mantel test, multiple matrix regression with randomization (MMRR) test and redundancy analysis (RDA). Here, six models were examined (Table 1): (a) IBDe, the geographical distance between populations was represented by Euclidian distance, which assumed the two Apodemus might disperse across the basin; (b) IBDr, the geographical distance between populations was represented by ring distance, which assumed no gene flow across the uninhabitable area in the centre of the ring; (c) IBE; (d) IBD+IBE, a model combining geographical and environmental variables; (e) IBD‐IBE, a model with the isolated effect of geographical variables when controlling for environmental variables; and (f) IBE‐IBD, a model with the isolated effect of environmental variables when controlling for geographical variables.…”

“…IBE implies that genetic divergence increases with environmental heterogeneity (Wang & Bradburd, 2014). We used three complementary statistical methods that are widely used to investigate the correlation between genotypes and geographical and environmental components (Forester et al, 2018;Huang et al, 2016;Kierepka & Latch, 2015;Wang, 2013;Yang et al, 2020), namely the Mantel test, multiple matrix regression with randomization (MMRR) test and redundancy analysis (RDA). Here, six models were examined (Table 1) variables.…”

Approved Genetically Modified Potatoes (Solanum tuberosum) for Improved Stress Resistance and Food Safety

“…Adult CPB can overwinter in the soil for a period of at least 30 days. After this period (in spring), they are ready to disperse, preferring to walk over flight to the host . Females can lay up to 800 eggs during their lifetime.…”