Study On The Genetic Differentiation Mechanism Of Potato Beetle Populations In Invaded Area

Colorado potato beetle(CPB),Leptinotarsa decemlineata,belongs to Coleoptera,is a quarantine invasive pest in the world,causing serious damage to the global potato industry and threatening major potato producing areas of China.Using population genetics method,this study investigated the genetic diversity,genetic structure,and genetic differentiation of CPB populations at two spatial scales: the invasion front(near northwest Xinjiang,China,based on 15 geographic populations and 9 microsatellite loci)and the Eurasian(based on based on 20 geographic populations and dd RAD sequencing),respectively.We further explored the formation mechanism of genetic differentiation: In the invasion front,this study combined landscape factors,such as geography,topography,climate,to explore the landscape factors that affect the genetic differentiation during the invasion process.In Eurasia,this study used population genomics method,combining with continental-scale climate data,to explore the environmental adaptation mechanism of CPB in Eurasia,thereby providing further insights into the mechanisms of successful invasions.The main results are as follows:1.The genetic diversity has declined substantially after invasion to Eurasia and invasion front.The allele richness at Microsatellite loci showed that the European population decreased by nearly 50% and the Asian population by nearly 80% compared with the native US population.Population genome data show that the effective population has fallen sharply from around 20,000 to several hundred when it invaded from the US to Europe.Based on microsatellite data,3 genetic groups were revealed in Eurasia,two of which were at the invasion front;Based on genomic data,8 genetic groups were revealed in Eurasia,of which 3 were at the invasion front.Overall,both Bayesian clustering and Principal Component Analysis showed weak genetic differentiation in most European populations.However,Asian populations,especially in the invasion front region of Xinjiang,China,showed relatively clear genetic differentiation.Multi-year sampling of the front populations found that such pattern of genetic divergence was formed in the early stages of invasion.2.Influencing factors of genetic differentiation of populations at the invasion front were revealed.The estimated effective migration surface showed that the gene flow in this area roughly matched the topography.The analyses of distance,environmental,and three kinds of resistances(suitable area,cropland cover,and transportation network)isolation models showed that isolation by resistance based on cropland connectivity had the highest correlation with the pattern of genetic divergence.Therefore,the cropland connectivity is the key to the successful invasion of CPB.Accordingly,this study mapped the least-cost dispersal path of CPB at the invasion front to reflect its invasion path.The findings shed light on the CPB’s invasion path and help guiding land management to slow further invasion of this pest.3.Elucidated the adaptation mechanism of CPB to the climate in Eurasia.This study found that the warmest seasonal average and annual average temperature are the main climatic factors shaping the genomic divergence of the Eurasian populations.The adaptive evolution to these two climate factors involved multiple genes and four major gene functions: methylation activity,redox reaction activity,transcription activity,and expression activity of phospholipid-related genes.This result suggests that there are multiple redundant genes and molecular mechanisms in the evolution of climatic adaptation.4.This study proposes that genetic redundancy may be a new mechanism to explain the genetic paradox of species invasion.The results of a new test to detect genetic redundancy found that in all Eurasian populations,the frequencies of many climate-adaptive loci did not obey the climatic gradient,that is,the frequencies in some populations did not correspond to the climatic conditions of the population.It suggests that these loci were not functioning in parts of the populations.Moreover,this study also found that different genes achieved the same gene function in climate adaptation.These results suggest that the corresponding adaptive genes are redundant for overall fitness.This study concludes that genetic redundancy promotes climate adaptation in Colorado potato beetle and may be a new mechanism to explain the genetic paradox of invasion.Taken together,this study demonstrated that landscape and environmental factors jointly promoted the genetic divergence of invasive CPB,but the relative extent of the two effects varied by the studied spatial scale.Regional studies and pest management should pay more attention to local topographic patterns and landscape configurations,while continental studies should pay more attention to the adaptation mechanisms of how CPB can widely spread.