Testing the Neogene grassland hypothesis: opposing macroevolutionary responses to environmental changes in grasses and insects

Authors: KERGOAT, GAEL - Non ARS Employee; CONDAMINE, FABIEN - University Of Montpellier; TOUSSANIT, EMMANUEL F. - University Of Florida; CAPDEVIELL-DULAC, CLAIRE - Universite Paris Descartes; CLAMENS, ANNE-LAURE - Non ARS Employee; BARBUT, JEROME - The Museum; Goldstein, Paul; LE RU, BRUNO - International Centre Of Insect Physiology And Ecology

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2018
Publication Date: 11/30/2018
Citation: Kergoat, G., Condamine, F.L., Toussanit, E.A., Capdeviell-Dulac, C., Clamens, A., Barbut, J., Goldstein, P.Z., Le Ru, B. 2018. Testing the Neogene grassland hypothesis: opposing macroevolutionary responses to environmental changes in grasses and insects. Proceedings of the National Academy of Sciences. 9(5089).

Interpretive Summary: Grasses account for an enormous proportion of human agriculture and invasive species alike, and insects that feed on grasses are of economic importance as both pests and biocontrol agents. Although many such species have arisen among groups of general plant feeders, large groups of grass-feeding specialist insects are important for our understanding how grass-feeding arose and whether we can use that understanding to predict or mitigate threats. Many such insect (and mammal) groups first appeared alongside C4 grasses, such as the ancestors of corn, during the massive spread of grasslands in Africa beginning roughly 20 million years ago. Using a combination of comparative DNA analyses and dating tools, we examine an economically important group of stem-boring moths diversified in parallel with grasses and the atmospheric factors that may have driven their spread and their dietary and feeding habits. We find that although C4 grasses continued to diversify with drops in temperature, the reverse pattern appeared in the insects that feed on them. This study challenges the conventional thinking that grasslands acted uniformly as "adaptive zones", suggesting a more complex picture in which a combination of biological and environmental features shape the origins of insects and insect pests. The work is of interest to prairie and grassland biologists, ecologists, paleontologists, range managers, agricultural and biocontrol scientists.

Technical Abstract: The role of Neogene grasslands in the origins and diversification of herbivores remains elusive due to inconsistent empirical evidence. Grasslands have been proposed as an adaptive zone sensu Simpson, and as a major ecological opportunity that may have boosted evolutionary rates in specialized herbivore lineages. We test this hypothesis with a novel model system, the Sesamiina stemborer moths and their associated host-grasses. This study builds upon an ecological dataset developed from 13 years of fieldwork in 17 sub-Saharan countries, and a molecular dataset comprising six loci for 1,393 specimens for 245 moth species. Using a comparative phylogenetic framework for the insects and their host-plants, we find a synchronous geographic and temporal origin for the two groups, suggesting that they interacted and diversified in parallel. We find strong evidence that, following the origin of both clades, speciation rates of insects decreased while those of grasses increased through time. Our results revealopposing macroevolutionary responses to environmental changes with temperature as a primary evolutionary driver. This study confirms that the drop of atmospheric carbon is a key driver for the diversification of C4 grasses. Analyses using organic carbon concentration as a proxy for the proportion of C4 grasses also indicate that the expansion of C4 grasslands did not act as a primary environmental driver for the insects. This study therefore calls into question the role of grasslands as a universal adaptive cradle, suggesting that the rise of C4 grasslands did not necessarily favor the diversification of herbivores that feed on them.