The evolutionary process of invasion in the fall armyworm (Spodoptera frugiperda)

Authors: YAINNA, SUDEEPTHA - University Of Montpellier; TAY, WEE TEK - Csiro, Black Mountain Laboratories; FITENI, ESTELLE - University Of Montpellier; FRAYSSINET, MARIE - University Of Montpellier; LEGEAI, FABRICE - Genoscope; CLAMENS, ANNE-LAURE - University Of Montpellier; GIMENEZ, SYLVIE - University Of Montpellier; KALLESHWARASWAMY, CM - Icar-Indian Institute Of Maize Research; ASOKAN, R - Icar-Indian Institute Of Maize Research; Meagher, Robert - Rob; BLANCEO, CARLOS - Animal And Plant Health Inspection Services (APHIS), National Wildlife Center; SILVIE, PIERRE - Cirad, France; BREVAULT, THIERRY - Cirad, France; DASSOUU, ANICET - University Of Benin; KERGOAT, GAEL - University Of Montpellier; WALSH, THOMAS - Csiro, Black Mountain Laboratories; GORDON, KARL - Csiro, Black Mountain Laboratories; NEGRE, NICHOLAS - University Of Montpellier; D'ALENCON, EMMANUELLE - University Of Montpellier; NAM, KIWOONG - University Of Montpellier

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/30/2022
Publication Date: 12/6/2022
Citation: Yainna, S., Tay, W.T., Durand,K., Fiteni, E., Hilliou, F., Legeai, F., Clamens, A., Gimenez, S., Asokan, R., Kalleshwaraswamy, C., Deshmukh, S.S., Meagher Jr, R.L., Blanceo, C.A., Silvie, P., Brevault, T., Dassouu, A., Kergoat, G.J., Walsh, T., Gordon, K., Negre, N., D'Alencon, E., Nam, K. 2022. The evolutionary process of invasion in the fall armyworm (Spodoptera frugiperda). Scientific Reports. 12:21063. https://doi.org/10.1038/s41598-022-25529-z.
DOI: https://doi.org/10.1038/s41598-022-25529-z

Interpretive Summary: Fall armyworm -is a highly polyphagous insect pest, native to the Western hemisphere. The invasion of the fall armyworm was first reported from West Africa in early 2016. In four years, the fall armyworm quickly swept through most of sub-Saharan Africa and Asia, finally reaching Australia in early 2020. Understanding how invasive populations survive, if not thrive, in new environments despite a reduced pool of diverse genetic traits is critical to understanding how to develop control methods for invasive populations. Scientists with the University of Montpellier, France, CSIRO, Australia, in collaboration with a scientist from USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, genetically analyzed samples of the fall armyworm that were field collected in the Western and Eastern Hemispheres to assess the genetic diversity of nuclear and mitochondrial genomes. The findings showed that the fall armyworm was able to produce new genetically stable local populations soon after invading a new environment which may facilitate the successful overtaking large areas of land.

Technical Abstract: A successful biological invasion involves survival in a novel environment. If a population bottleneck occurs during an invasion, the depletion of genetic variants may cause increased inbreeding depression and decreased adaptive potential, potentially causing decreased fitness in the invasive population. How invasive populations survive in a novel environment despite reduced heterozygosity and how, in many cases, invasive populations maintain moderate levels of heterozygosity is a contentious issue (1). The fall armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is a highly polyphagous insect pest, native to the Western hemisphere. The invasion of the fall armyworm was first reported from West Africa in early 2016. In four years, the fall armyworm quickly swept most of sub-Saharan Africa and Asia, finally reaching Australia in early 2020. Using population genomics on both native and invasive populations, we show that in the fall armyworm, genomic balancing selection played a key role in establishing a stable invading population, which is a source of further explosive global invasion. We observed a drastic loss of polymorphisms in mitochondrial DNA, whereas nuclear heterozygosity shows only a mild reduction in invasive populations. The population from West Africa (Benin) has the lowest length of linkage disequilibrium among all invasive and native populations despite reduced effective 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 high enough, it allows the fall armyworm to spread globally in the Old World. As comparable heterozygosity levels between invasive and native populations are commonly observed, we raise the possibility that the restoration of heterozygosity through balancing selection could be widespread among successful invasive species.