The opening of habitats associated with the emergence of C4 grasslands during the Neogene has had a massive influence on the evolution of plant and animal communities. Strikingly, the impacts of grassland expansion on species diversification in Africa, where the largest surface of grasslands and savannas in the world is located, are not well understood. To explore the impact of habitat opening, we investigate the evolution of noctuid stemborers, a group of moths mostly associated with open habitats, and whose diversity is centered in the Afrotropics. We generate a dated molecular phylogeny for ca. 80% of the known stemborer species and assess the role of habitat opening on the evolutionary trajectory of the group through a combination of parametric historical biogeography, ancestral character state estimation, life history traits and habitat-dependent diversification analyses. Our results support an origin of stemborers in Southern and East Africa ca. 20 million years ago (Ma), with range expansions linked to the increased availability of open habitats to act as dispersal corridors, and closed habitats acting as potent barriers to dispersal. Early specialization on open habitats was maintained over time, with shifts towards closed habitats being rare and invariably unidirectional. Analyses of life history traits showed that habitat changes involved specific features likely associated with grassland adaptations, such as variations in larval behavior and color. We compare these findings to those previously inferred for an Afrotropical butterfly group that diversified roughly in parallel with the stemborers but distributed predominantly in closed habitats. Remarkably, these two groups show nearly opposite responses in relation to habitat specialization, whether in terms of biogeographical patterns, or in terms of rates of transition between open and closed habitats. We conclude that habitat opening played a major role in the diversification of Afrotropical lineages through dispersal and adaptation linked to habitat shifts.

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 increase inbreeding depression and decreased adaptive potential, potentially resulting in the extinction. How invasive populations survive and thrive in a newly occupied environment and how, in many cases, they maintain moderate levels of heterozygosity are still contentious issues. The pest Fall armyworm (FAW; Lepidoptera: Spodoptera frugiperda) is native to the Western hemisphere. Its invasion in the Eastern hemisphere 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. In this study, we used population genomics approaches to investigate the factors explaining the invasive success of the FAW. We observe a drastic loss of mitochondrial polymorphisms 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 supports that balancing selection increased heterozygosity by facilitating the admixture of invasive populations from distinct origins and that, once heterozygosity was sufficiently high, the FAW started spreading globally in the Eastern hemisphere. As comparable heterozygosity levels between invasive and native populations are commonly observed, we postulate that heterozygosity restoration through balancing selection could be widespread among successful cases of biological invasions.