Genomic evidence of speciation by fusion linked to trophic niche expansion in a recent radiation of grasshoppers

Abstract

Post-divergence gene flow can trigger a number of creative evolutionary outcomes, ranging from the transfer of beneficial alleles across species boundaries (i.e., adaptive introgression) to the formation of new species (i.e., hybrid speciation). While neutral and adaptive introgression has been broadly documented in nature, hybrid speciation is assumed to be rare and the evolutionary and ecological context facilitating this phenomenon still remains controversial. Through combining genomic and phenotypic data, we evaluate the hypothesis that the dual feeding regime (scrub legumes and gramineous herbs) of the taxonomically controversial grasshopper Chorthippus saulcyi algoaldensis resulted from hybridization between two sister taxa that exhibit contrasting host-plant specializations: C. binotatus (scrub legumes) and C. saulcyi (gramineous herbs). Genetic clustering analyses and inferences from coalescent-based demographic simulations confirmed that C. s. algoaldensis represents a uniquely evolving lineage and supported the ancient hybrid origin of this taxon (ca. 1.4 Ma), which provides a mechanistic explanation for its broader trophic niche and sheds light on its uncertain phylogenetic position. We propose a Pleistocene hybrid speciation model where range shifts resulting from climatic oscillations can promote the formation of hybrid swarms and facilitate its long-term persistence through geographic isolation from parental forms in topographically complex landscapes.