Host-plant adaptation as a driver of incipient speciation with gene flow in the fall armyworm (Spodoptera frugiperda)

Authors: FITENI, ESTELLE - University Of Montpellier; DURAND, KARINE - University Of Montpellier; GIMENEZ, SYLVIE - University Of Montpellier; Meagher, Robert - Rob; LEGEAI, FABRICE - National Research Institute For Agriculture, Food And Environment; KERGOAT, GAEL - National Research Institute For Agriculture, Food And Environment; NEGRE, NICHOLAS - University Of Montpellier; D'ALENCON, EMMANUELLE - University Of Montpellier; NAM, KIWOONG - University Of Montpellier

Submitted to: BMC Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2022
Publication Date: 11/11/2022
Citation: Fiteni, E., Durand, K., Gimenez, S., Meagher Jr, R.L., Legeai, F., Kergoat, G.J., Negre, N., D'Alencon, E., Nam, K. 2022. Host-plant adaptation as a driver of incipient speciation with gene flow in the fall armyworm (Spodoptera frugiperda). BMC Ecology and Evolution. 22:133. https://doi.org/10.1186/s12862-022-02090-x.
DOI: https://doi.org/10.1186/s12862-022-02090-x

Interpretive Summary: The fall armyworm, Spodoptera frugiperda, is now a worldwide pest that causes significant economic damage to a variety of crops in the Americas, Africa, Asia, and Australia. This species is composed of two host strains, corn and rice (or grass), named after their preferred host-plants. Scientists speculate that these two strains are undergoing speciation, where the corn strain will become a separate species from the rice strain. Geneticists from several universities and institutes in France along with an USDA-ARS Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, entomologist, collected fall armyworm caterpillars from corn and grass pastures in Florida. The DNA from these caterpillars was used to conduct several genetic analyses. Results of the tests showed that the corn and grass populations were genetically different and that these differences were contributing to separating the populations into different species. Previous studies have shown that the two host strains differ in Bacillus thuringiensis and insecticide susceptibility. Thus knowing which host strain is attacking your crops can help you determine which control method will be the most effective.

Technical Abstract: Divergent selection on host-plants is one of the main evolutionary forces driving ecological speciation in phytophagous insects. This ecological speciation might be challenging in the presence of gene flow and assortative mating because the direction of divergence is not necessarily the same between ecological selection (through host-plant adaptation) and assortative mating. The fall armyworm (FAW), a major lepidopteran pest species, is composed of two sympatric strains, corn and rice strains, named after two of their preferred host-plants. These two strains have been hypothesized to undergo incipient speciation, on the basis of, (i) several lines of evidence encompassing both pre- and post-zygotic reproductive isolation, and (ii) the presence of a substantial level of genetic differentiation. Even though the status of these two strains has been established a long time ago, it is still yet to be found whether these two strains indeed exhibit a marked level of genetic differentiation from a large number of genomic loci. Here, we analyzed whole genome sequences from 56 FAW individuals either collected from pasture grasses (a part of the favored host range of the rice strain) or corn to assess the role of host-plant adaptation in incipient speciation. Principal component analysis of whole genome data shows that the pattern of divergence in the fall armyworm is predominantly explained by the genetic differentiation associated with host-plants. The level of genetic differentiation between corn and rice strains is particularly marked in the Z chromosome. We identified one autosomal locus and two Z chromosome loci targeted by selective sweeps specific to rice strain and corn strain, respectively. The autosomal locus has both increased DXY and FST. while the Z chromosome loci had decreased DXY and increased FST. These results show that the FAW population structure is dominated by the genetic differentiation between analyzed corn and rice strains. This differentiation was initiated by autosomal divergent selection in the rice strain and then strengthened by Z chromosome divergent selection in the corn strain. Taken together, these results suggest the evolutionary scenario that host-plant speciation is a driver of incipient speciation in the fall armyworm.