Population Genetic Structure And Adaptative Genetic Variation Of The Invasive Mealybug Phenacoccus Solenopsis In China

A growing number of studies suggest that evolutionary adaptation of invasive species play key roles in their successful establishment in novel environments.However,adaptation of invasive species to climatic conditions remains poorly characterized.Phenacoccus solenopsis,the cotton mealybug has became a serious pest across China since its introduction ten years ago.In this study,we examined population structure,genetic diversity and adaptive evolution of 11 populations of P.solenopsis based on microsattelite DNA and single nucleotide polymorphism markers.Results and conclusions were as followed.1.Development of novel microsatellites and genetic diversity of P.solenopsisWe generated a draft genome from a DNA library by sequencing on an Illumina Hiseq4000 system.The length of total scaffolds was 267.07 Mb,with longest scaffold of 317.8 Kb,scaffold N50 of 14.12 Kb,and the estimated completeness of the genome was 89.6%.Based on the draft genome,42 primer pairs generated.Of which two loci（PS3-S23 and PS4-S16）fell into the candidate space for balancing selection,while others fell into space consistent with neutral expectations.The specific markers developed provide efficient molecular tools for P.solenopsis.We analyzed genetic diversity based on microsatellites.Observed heterozygosity（H_O）and expected heterozygosity（H_E）ranged from 0.0 to 0.9 and 0.00 to 0.7,respectively.Allele numbers varied from 2 to 5 and allelic richness ranged from 1.0 to 4.5.The polymorphism information content（PIC）of the loci ranged from 0.0 to 0.5.In the Jiangxi population,three loci showed deviations from Hardy-Weinberg equilibrium（HWE）（P<0.05）.Seven loci showed deviation from HWE in the Guangdong and Jiangsu populations,and two loci（PS4-S27 and PS5-S34）deviated significantly in both populations.In addition,13 pairs of loci showed significant linkage disequilibrium（LD）（P<0.01）in all populations.2.Characterization of SNPs and genetic diversity analysisFor ddRAD library,average raw reads depths was 37.18X and mapping rate was95.07%.In total,we obtained 19,634 SNPs among 11 populations of P.solenopsis,including2,117 outliers and 17,517 neutral loci.Based on SNPs,observed heterozygositywere larger than expected heterozygosity.The inbreeding coefficient(F_IS)of populations are negative.The nucleotide diversity（Pi）ranged from 0.1 to 0.3.Polymorphism（%）varied from 0.0 to 0.2.3.Genetic structure and invasion history of P.solenopsisBased on neutral SNPs,we found Fst was significantly higher in Xijiang compared to other groups（P<0.001）,and pairwise distances in all populations with more than 0.0.ADMIXTURE analysis identified optimal K as 11.When K=11,each populations separated respectively.DAPC analysis showed XJTL and FJPT were clustered into two separate groups,other populations were assembled into a cluster.Phylogenetic analyses showed HNCS,HNYY,JXNC,and JXGZ were closely related indicating higher relatedness among populations.XJTL and AHHF had stronger differentiated than among others.Despite the cotton mealybug only have introduced to China for fewer years,there was rapid differentiation between populations.DIYABC analysis based on microsatellites showed that XJTL might be introduced by a single event from southern populations.4.Adaptive evolution of P.solenopsisIn XJTL population,numbers of private alleles were abundant,while Pi values were lower.In addition,population structure and diversity based on outliers were consistent with the results based on neutral loci.Redundant analysis showed that climate variables accounted for 58.9%of the total explained variance in SNP genotypes,while geographical variables explained 13.1%of that.The top climatic variables identified to be associated with SNP variations were BIO14（Precipitation of driest month）,BIO5（Max temperature of warmest month）and BIO9（Mean temperature of driest quarter）.Enrichment analysis on genes of associated SNPs obtained 61 pathways mainly related to development,energy and xenobiotic metabolisms.In summary,our study on the population genetics of a invasive species P.solenopsis revealed three major findings on the invasion of this species.First,the data are consistent with the invasive species invading China from a single source population.Second,extremely rapid and strong population genetic differentiation among populations appears to have developed after introduction,suggesting limited gene flow,and small effective population sizes.Third,we found suggestive evidence of genomic signatures of climatic adaptation in a invasive species despite very low genetic diversity in the introduced population.