Genomic balancing selection is key to the invasive success of the fall armyworm

Abstract

A successful biological invasion involves survival in a newly occupied environment. If a population bottleneck occurs during an invasion, the resulting depletion of genetic variants could cause increased inbreeding depression and decreased adaptive potential, which may result in a fitness reduction. How invasive populations survive in the newly occupied environment despite reduced heterozygosity and how, in many cases, they maintain moderate levels of heterozygosity are still contentious issues 1 . The Fall armyworm (FAW; Lepidoptera: Spodoptera frugiperda), a polyphagous pest, is native to the Western hemisphere. Its invasion in the Old World was first reported from West Africa in early 2016, and in less than four years, it swept sub-Saharan Africa and Asia, finally reaching Australia. We used population genomics approaches to investigate the factors that may explain the invasive success of the FAW. Here we show that genomic balancing selection played a key role in invasive success by restoring heterozygosity before the global invasion. We observe a drastic loss of mitochondrial polymorphism in invasive populations, whereas nuclear heterozygosity exhibits a mild reduction. The population from Benin in West Africa has the lowest length of linkage disequilibrium amongst all invasive and native populations despite its reduced population size. This result indicates that balancing selection increased heterozygosity by facilitating the admixture of invasive populations from distinct origins and that, once heterozygosity was sufficiently high, FAW started spreading globally in the Old World. As comparable heterozygosity levels between invasive and native populations are commonly observed 1 , we postulate that the restoration of heterozygosity through balancing selection could be widespread among successful cases of biological invasions.

Global FAW population genomic signature supports complex introduction events across the Old World

“…The early detections and report of FAW in Asia/S.E. Asia (e.g., CH06 from this study from 2016, see GenBank record MT897262; 2008 FAW outbreaks on turf grass in Hà Nội 106 ), and the complex pattern of multiple introductions as evident from genomic signatures (e.g., this study; Yainna et al 69 ), are consistent with the perceived rapid spread experienced across the African 110 and Asian continents 111 .…”

“…For example, copy number variations (CNV) analysis from whole genome sequence data 38 also detected distinct signatures between the China/East African (Uganda, Malawi) from the Benin/Indian FAW populations, thereby further supported multiple introductions of FAW across different Old World regions. This and the study of Yainna et al 69 highlight the need for whole-genome derived datasets to accurately trace population origins and global movements of highly mobile insect pests.…”

“…The other test for neutrality, Fu & Li’s D*, gave consistent results with Tajima‘s D, further supporting the finding of genomic signatures in these populations due to recent introduction of different populations. These demographic factors are the likely reason for the elevated neutrality test results, since these were averages across the complete SNP set derived from the whole genome, rather than results for individual loci that might be under balancing selection 69 . Interestingly, this may also apply to populations in the native range.…”

“…Total genomic DNA from Mississippi, Florida, Puerto Rico, Guadeloupe, Mexico, and French Guiana, and Indian populations was carried out at INRAE DGIMI (Univ. Montpellier, INRAE, France) as described in Yainna et al 69 .…”

“…The reference genomes 44 are from native populations, Sf C from Guadeloupe and Sf R from Florida (see also Yainna et al 69 , and Nam et al 68 for high quality assemblies of native population genomes for Sf R, and Nam et al 76 for high quality genome assemblies of native Sf c). The reference genomes published recently by three Chinese groups may differ since they are from invasive populations, from Yunnan in China 77 , from the Zhejiang province of China 78 , and from 2017 sampled FAW individuals collected from maize fields in Lusaka, Zambia 45 .…”