Genomic Evidence of Speciation by Fusion in a Recent Radiation of Grasshoppers

Postdivergence 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). Although 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 (based on both scrub legumes and gramineous herbs) of the taxonomically controversial grasshopper Chorthippus saulcyi algoaldensis resulted from hybridization between the sister taxa C. binotatus (that exclusively feeds on scrub legumes) and C. saulcyi (that only feeds on gramineous herbs). Genetic clustering analyses and inferences from coalescent-based demographic simulations confirm that C. s. algoaldensis represents an independently evolving lineage and support the ancient hybrid origin of this taxon (about 1.4 Ma), which sheds light on its uncertain phylogenetic position and might explain its broader trophic niche. We propose a Pleistocene hybrid speciation model where range shifts resulting from climatic oscillations can promote the formation of hybrid swarms and facilitate their long-term persistence through geographic isolation from parental forms in topographically complex landscapes.