Abstract

AbstractAimA growing number of studies suggest that adaptation of invasive species plays key roles in their successful establishment in novel environments. However, adaptation of invasive species to climatic conditions remains poorly characterized. This study aimed to understand the population genetic structure produced by the cotton mealybug Phenacoccus solenopsis invasion and to identify preliminary signals of selection during its range expansion.LocationChina.MethodsWe examined genetic structure of 11 populations across China using SNPs, microsatellites and a segment of mitochondrial cox1 gene. ADMIXTURE, STRUCTURE and DAPC were used to infer population genetic structure; the dispersal routes were reconstructed by the DIYABC; SNPs potentially related to climate adaptation were identified by using four populations differentiation methods and three environmental association methods.ResultsStrong genetic differentiation was found among populations with FST values ranging from 0.097 to 0.640 based on SNPs. Populations located at the northern expansion edge exhibited the highest genetic differentiation and the lowest genetic diversity. Demographic analyses indicated that all populations were introduced from a single source population with small effective size and low recent gene flow. RDA analysis showed that climatic variables explained a higher proportion of genetic variance (43%) compared to population structure variables (15%). The top climatic variables associated with genetic differentiation were precipitation of the mean temperature of warmest quarter, mean temperature of driest quarter and isothermality. Genes related to climate candidate SNPs were mainly enriched to pathways of development, energy and xenobiotic metabolisms.Main conclusionsWe found that extremely rapid and strong population genetic differentiation among populations appears to have developed after introduction in the cotton mealybug. Our study points to rapid neutral evolution and suggests possible climatic adaptation despite low genetic diversity in this invasive species.

Highlights

  • Invasive species commonly show a high potential to spread across vast geographical areas with diverse environmental conditions (Seebens et al, 2017)

  • There was no significant departure from Hardy–Weinberg equilibrium (HWE) and linkage disequilibrium for a locus in all populations or a population on all loci, except for deviations from HWE in FJTP and GDGZ based on all microsatellites (p < .01) (Table S5)

  • The double-digest restriction site-associated DNA (ddRAD) approach provides an efficient method to develop high-throughput SNPs, including potentially neutral and selected loci (Pujolar et al, 2013); the microsatellites provided a supplement to SNPs for making neutral process inferences, such as about population genetic structure and demographic history; the mitochondrial cox1 gene helped to validate the morphological identification of the species

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Summary

Introduction

Invasive species commonly show a high potential to spread across vast geographical areas with diverse environmental conditions (Seebens et al, 2017). Previous studies showed that these species usually exhibit higher phenotypic plasticity than native species (Amy Michelle, Michael, & Nicotra, 2011; Felden et al, 2018; Vanwallendael et al, 2018), helping them to colonize new areas Both theoretical and empirical studies suggest that invasive populations of many species are expected to undergo evolutionary adaptation to respond to new conditions (Andrew, Jensen, Hagen, Lundregan, & Griffith, 2018; Lee, 2002; Renault et al, 2018; van Boheemen & Atwater, 2019; Willoughby et al, 2018). This means that invasive populations provide an opportunity to understand and contrast population evolution under both neutral (bottlenecks, gene flow) and adaptive processes (Bock et al, 2015; Lee, 2002)

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