Global patterns of genomic and phenotypic variation in the invasive harlequin ladybird

• Published in: BMC biology Vol. 21; no. 1; p. 141
• Main Authors: Li, Hongran, Peng, Yan, Wang, Yansong, Summerhays, Bryce, Shu, Xiaohan, Vasquez, Yumary, Vansant, Hannah, Grenier, Christy, Gonzalez, Nicolette, Kansagra, Khyati, Cartmill, Ryan, Sujii, Edison Ryoiti, Meng, Ling, Zhou, Xuguo, Lövei, Gábor L, Obrycki, John J, Sethuraman, Arun, Li, Baoping
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 19-06-2023; BioMed Central; BMC
• Subjects: Adaptation; Analysis; Animal introduction; Animals; Beetles; Biodiversity; Biological Variation, Population; Coleoptera - genetics; Colonization; Color vision; Continents; Dispersal; Distribution; Evolutionary history; Genetic aspects; Genomes; Genomic analysis; Genomics; Haplotypes; Harmonia axyridis; Hemolymph; Insect pests; Insects; Invasion biology; Invasive insects; Invasive species; Invasiveness; Ladybirds; Life history; Migration; mtCOI; Natural history; Nonnative species; Phenotype; Phenotypic variations; Phylogenetics; Population; Population genomics; Population structure; Populations; Success; Visual perception; Zoological research; North America; China; Europe; America; South America; Life history; mtCOI; Invasion biology; Evolutionary history; Population genomics; Adaptation
• ISSN: 1741-7007; 1741-7007
• DOI: 10.1186/s12915-023-01638-7

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae), native to Asia, has been introduced to other major continents where it has caused serious negative impacts on local biodiversity. Though notable advances to understand its invasion success have been made during the past decade, especially with then newer molecular tools, the conclusions reached remain to be confirmed with more advanced genomic analyses and especially using more samples from larger geographical regions across the native range. Furthermore, although H. axyridis is one of the best studied invasive insect species with respect to life history traits (often comparing invasive and native populations), the traits responsible for its colonization success in non-native areas warrant more research.
Our analyses of genome-wide nuclear population structure indicated that an eastern Chinese population could be the source of all non-native populations and revealed several putatively adaptive candidate genomic loci involved in body color variation, visual perception, and hemolymph synthesis. Our estimates of evolutionary history indicate (1) asymmetric migration with varying population sizes across its native and non-native range, (2) a recent admixture between eastern Chinese and American populations in Europe, (3) signatures of a large progressive, historical bottleneck in the common ancestors of both populations and smaller effective sizes of the non-native population, and (4) the southwest origin and subsequent dispersal routes within its native range in China. In addition, we found that while two mitochondrial haplotypes-Hap1 and Hap2 were dominant in the native range, Hap1 was the only dominant haplotype in the non-native range. Our laboratory observations in both China and USA found statistical yet slight differences between Hap1 and Hap2 in some of life history traits.
Our study on H. axyridis provides new insights into its invasion processes into other major continents from its native Asian range, reconstructs a geographic range evolution across its native region China, and tentatively suggests that its invasiveness may differ between mitochondrial haplotypes.