Stable inversion clines in a grasshopper species group despite complex geographical history

Abstract

Chromosomal inversions are known to play roles in adaptation and differentiation in many species. They involve clusters of correlated genes (i.e., loci in linkage disequilibrium, LD) possibly associated with environmental variables. The grasshopper “species complex” Trimerotropis pallidipennis comprises several genetic lineages distributed from North to South America in arid and semi-arid high-altitude environments. The southernmost lineage, Trimerotropis sp., segregates for four to seven putative inversions that display clinal variation, possibly through adaptation to temperate environments. We analysed chromosomal, mitochondrial and genome-wide single nucleotide polymorphism data in 19 Trimerotropis sp. populations mainly distributed along two altitudinal gradients (MS and Ju). Populations across Argentina comprise two main chromosomally and genetically differentiated lineages: one distributed across the southernmost border of the “Andes Centrales,” adding evidence for a differentiation hotspot in this area; and the other widely distributed in Argentina. Within the latter, network analytical approaches to LD found three clusters of correlated loci (LD-clusters), with inversion karyotypes explaining >79% of the genetic variation. Outlier loci associated with environmental variables mapped to two of these LD-clusters. Furthermore, despite the complex geographical history indicated by population genetic analyses, the clines in inversion karyotypes have remained stable for more than 20 generations, implicating their role in adaptation and differentiation within this lineage. We hypothesize that these clines could be the consequence of a coupling between extrinsic postzygotic barriers and spatially varying selection along environmental gradients resulting in a hybrid zone. These results provide a framework for future investigations about candidate genes implicated in rapid adaptation to new environments.