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

GUZMÁN, NOELIA V.; KEMPPAINEN, PETRI; MONTI, DANIELA; CASTILLO, ELIO R. D.; RODRIGUERO, MARCELA S.; SÁNCHEZ-RESTREPO, ANDRÉS F.; CIGLIANO, MARIA MARTA; CONFALONIERI, VIVIANA A.

MOLECULAR ECOLOGY

WILEY-BLACKWELL PUBLISHING, INC

Año: 2022

0962-1083

Chromosomal inversions are known to play roles in adaptation and differentiation inmany species. They involve clusters of correlated genes (i.e., loci in linkage disequilib-rium, LD) possibly associated with environmental variables. The grasshopper ?speciescomplex? Trimerotropis pallidipennis comprises several genetic lineages distributedfrom North to South America in arid and semi-­arid high-­altitude environments. Thesouthernmost lineage, Trimerotropis sp., segregates for four to seven putative inver-sions that display clinal variation, possibly through adaptation to temperate environ-ments. We analysed chromosomal, mitochondrial and genome-­wide single nucleotidepolymorphism data in 19 Trimerotropis sp. populations mainly distributed along twoaltitudinal gradients (MS and Ju). Populations across Argentina comprise two mainchromosomally and genetically differentiated lineages: one distributed across thesouthernmost border of the ?Andes Centrales,? adding evidence for a differentiationhotspot in this area; and the other widely distributed in Argentina. Within the lat-ter, network analytical approaches to LD found three clusters of correlated loci (LD-­clusters), with inversion karyotypes explaining >79% of the genetic variation. Outlierloci associated with environmental variables mapped to two of these LD-­clusters.Furthermore, despite the complex geographical history indicated by population ge-netic analyses, the clines in inversion karyotypes have remained stable for more than20 generations, implicating their role in adaptation and differentiation within thislineage. We hypothesize that these clines could be the consequence of a couplingbetween extrinsic postzygotic barriers and spatially varying selection along environ-mental gradients resulting in a hybrid zone. These results provide a framework forfuture investigations about candidate genes implicated in rapid adaptation to newenvironments.