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.

Comparative Genetic Analysis of Invasive Fall Armyworm Populations Provides Evidence for Population Expansion in India

“…One would be the uncharacteristic similarity between the ancestral population for all the invaded regions, which is indicative of a recent and a common source. Secondly, most of the earlier studies on FAW sequences in India have reported low levels of genetic variation, similar to the one found in Africa and East Asia [7,18,[21][22]. Thirdly, the distribution of the novel haplotypes in Indian populations is unimodal, typical of founder effect with recent population expansion.…”

“…In general, Tpi gene was found to accurately predict the host association in invasive populations [3,[18][19]. The discordance between the two markers was re ective of the hybrid nature of the invasive populations which was subsequently corroborated with whole genome studies [20][21]. Barring the detection of two maternal COI lineages and a limited number of Tpi haplotypes, genetic variability in the invasive populations was found to be very low.…”

“…But it is important to understand that COIA'R' strain found in India or other recently invaded countries does not represent the true ancestral 'R' strain. Multiple studies have suggested it to be a hybrid strain as marked by the discordance between Tpi and COIA markers and by other genome sequencing studies [18,[20][21]. Thus, the behaviour of this population is not well characterised and the mating barriers between this population and the ancestral strains are also not yet known.…”

“…Spodoptera frugiperda provides an excellent model system in this regard since it is believed to have expanded its distribution range very recently and has been well documented and characterised for its diversity in its native as well as the extended range. Most of the studies involving diversity of Indian FAW populations were performed around two years ago from few locations where it was rst detected in India [7,18,[21][22]. Thus we thought it was imperative to understand the diversity of Indian FAW population over the course of last two years after the expansive migration of FAW across India.…”

“…The Indian population exhibited high homogeneity with East and South African populations with the majority showing mitochondrial rice strain COI and nuclear corn strain Tpi marker [18]. Mitochondrial diversity of the analysed specimens was found to be very low when compared to the native population [7,21].…”