Opposite macroevolutionary responses to environmental changes in grasses and insects during the Neogene grassland expansion

Gael J Kergoat,Jérôme Barbut,Paul Z Goldstein,Anne-Laure Clamens,Claire Capdevielle-Dulac,Bruno Le Ru,Fabien L Condamine,Emmanuel F A Toussaint

doi:10.1038/s41467-018-07537-8

Abstract

The rise of Neogene C4 grasslands is one of the most drastic changes recently experienced by the biosphere. A central - and widely debated - hypothesis posits that Neogene grasslands acted as a major adaptive zone for herbivore lineages. We test this hypothesis with a novel model system, the Sesamiina stemborer moths and their associated host-grasses. Using a comparative phylogenetic framework integrating paleoenvironmental proxies we recover a negative correlation between the evolutionary trajectories of insects and plants. Our results show that paleoenvironmental changes generated opposing macroevolutionary dynamics in this insect-plant system and call into question the role of grasslands as a universal adaptive cradle. This study illustrates the importance of implementing environmental proxies in diversification analyses to disentangle the relative impacts of biotic and abiotic drivers of macroevolutionary dynamics.

Highlights

The rise of Neogene C4 grasslands is one of the most drastic changes recently experienced by the biosphere
Our study shows that differential responses to environmental changes may yield counter-intuitive patterns of diversification in plants and insects
The initial radiation of C4 grasses in the Afrotropics likely met criteria for an adaptive zone in a group of grass-specialist insects, subsequent climatic changes may have driven diversification in a direction opposite that predicted by the inferred spread of C4 grasslands ca. 3–9 million years ago (Ma)

Summary

Introduction

The rise of Neogene C4 grasslands is one of the most drastic changes recently experienced by the biosphere. Fossil phytoliths and paleosols support this hypothesis, indicating that C4 grasses appeared about 20–25 Ma in the geological record[5] This pattern is confirmed by recent molecular phylogenetic studies, which indicate that distinct C4 grass lineages appeared multiple times between the late Oligocene and the late Miocene[1], and that the shift from C3 to C4 pathways constituted an important precursor to speciation in the evolutionary history of grasses[6]. A commonly accepted theory posits that the Neogene grasslands enabled the development of adaptive radiations, favouring lineages of grass eaters following key innovations in dental morphology (hypsodonty), and plant assimilation[18] This view was recently challenged by studies revealing that hypsodonty originated well before the appearance and spread of Neogene grasslands We could postulate that the diversification of specialized herbivores may be unaffected by host diversification, if they remain able to utilize all the descendant hosts of their ancestral host-plants

Methods

Results

Conclusion