Rapid and strong population genetic differentiation and genomic signatures of climatic adaptation in an invasive mealybug

Abstract

Aim A 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. Location China. Methods We 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. Results Strong 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 conclusions We 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.

Local climate adaptation and gene flow in the native range of two co‐occurring fruit moths with contrasting invasiveness

“…Gene flow within a native range may also promote the invasiveness of species by producing admixture from different sources that could facilitate the evolution of novel phenotypes (van Boheemen et al, 2017). Nevertheless, some successful invaders can establish their populations in newly colonized areas following a single introduction (Cao et al, 2016; Ma et al, 2020).…”

Genomic signatures of admixture and selection are shared among populations of Zaprionus indianus across the western hemisphere

“…As such, understanding the demographic and evolutionary origins of introduced species is important if we are to understand evolution and biodiversity in the Anthropocene. Research has shown how introduced populations can rapidly differentiate from populations in their native range and adapt to their introduced range (Dupuis et al, 2018;Koch et al, 2020;Ma et al, 2020;Stuart et al, 2021;Zayed & Whitfield, 2008);…”

“…As such, understanding the demographic and evolutionary origins of introduced species is important if we are to understand evolution and biodiversity in the Anthropocene. Research has shown how introduced populations can rapidly differentiate from populations in their native range and adapt to their introduced range (Dupuis et al, 2018 ; Koch et al, 2020 ; Ma et al, 2020 ; Stuart et al, 2021 ; Zayed & Whitfield, 2008 ); however, the origin of that adaptive variation is seldom known (however, see Calfee et al, 2020 ). In this manuscript, we leveraged genome sequences to provide evidence that introduced populations of Z .…”

“…Similar to admixture, populations of introduced species can experience selection at different times and locations during their range expansions and there is increasing evidence of rapid genetic differentiation consistent with selection acting within populations of introduced species (Dupuis et al, 2018 ; Koch et al, 2020 ; Ma et al, 2020 ; Stuart et al, 2021 ; Zayed & Whitfield, 2008 ). We found that populations of Z .…”

Microsatellite Variation in the Most Devastating Beetle Pests (Coleoptera: Curculionidae) of Agricultural and Forest Crops

“…Microsatellites, also known as simple sequence repeats (SSRs), are 1–6 bp motifs present in both coding and non-coding regions of eukaryotic and prokaryotic genomes that have become the primary source of genetic markers for population analysis in insects due to their high levels of polymorphism [ 13 ]. It is well established that SSRs have high rates of mutation and thus have implications for genome organization and genetic variation [ 14 , 15 ].…”