Habitat opening fostered diversity at both continental and local scales: impact of dispersal and habitat-shifts in the diversification of a speciose Afrotropical insect group

Authors: HEVIN, NOEMIE - University Of Montpellier; Goldstein, Paul; ADUSE-POKU, KWAKU - Georgia State University; BARBUT, JEROME - University Of Paris; MITCHELL, ANDREW - Australian Museum; ZILLI, ALBERTO - London Natural History Museum; CLAMENS, ANNE-LAURE - University Of Montpellier; CAPDEVIELLE-DULAC, CLAIRE - Université Paris-Saclay; WAHLBERG, NIKLAS - Lund University; LE RU, BRUNO - University Of Nairobi; KERGOAT, GAEL - Center For Biology And Management Of Populations

Submitted to: Systematic Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/1/2024
Publication Date: 6/13/2024
Citation: Hevin, N.M., Goldstein, P.Z., Aduse-Poku, K., Barbut, J., Mitchell, A., Zilli, A., Clamens, A., Capdevielle-Dulac, C., Wahlberg, N., Le Ru, B., Kergoat, G. 2024. Habitat opening fostered diversity at both continental and local scales: impact of dispersal and habitat-shifts in the diversification of a speciose Afrotropical insect group. Systematic Biology. 2024(8). Article e07258. https://doi.org/10.1111/ecog.07258.
DOI: https://doi.org/10.1111/ecog.07258

Interpretive Summary: This paper analyzes the largest phylogenomic dataset so far for the subtribe of Old World Stemborer moths, and traces their evolution beginning in southern and eastern Africa during the expansion of grasslands during the Miocene. We use these data to test evolutionary models at large and small scales, and conclude that the opening of grasslands and savannas drove diversification in this important pest clade. The Old World Stemborers exhibit a pattern of diversification opposite that of a well-studied genus of butterflies that evolved at roughly the same time in closed habitats. This work is of interest to entomologists, biogeographers, plant-herbivore scientists, and evolutionary biologists.

Technical Abstract: The opening of habitats associated with the emergence of C4 grasslands during the Neogene played a major role in biome evolution, influencing the evolution of numerous lineages on diverse scales. 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. These impacts may be investigated at large scales by examining extrinsic factors (Court Jester model), and at small scales through the consideration of more intrinsic biotic interactions (Red Queen model). To explore which of these applies, we investigate the evolution of noctuid stemborers (Lepidoptera: Noctuidae: Sesamiina), a group of moths mostly associated with open habitats, and whose diversity is mainly in the Afrotropics. We generate a dated molecular phylogeny for 229 stemborer species and further 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 (Mya), with range expansions linked to the increased availability of open habitats that acted as dispersal corridors, and closed habitats acting as potent barriers to dispersal. At a local scale, habitat opening fostered diversification, and the initial 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 led to or at least preceded specific adaptations, such as variations in larval behavior and color. We compare these findings to those previously inferred for Bicyclus brush-footed butterflies (Lepidoptera: Nymphalidae: Satyrinae), a butterfly group that diversified roughly in parallel but distributed mainly in closed habitats. Remarkably, these two groups exhibit nearly opposite patterns of diversification, both on a continental and local scale.