The genomic architecture of inversion clines in a grasshopper species
group with a complex biogeographic history
Abstract
Chromosomal inversions play a role in the adaptation and diversification
of different systems, mainly due to supergenes resulting from
recombination suppression. Supergenes are “clusters” of genes in
linkage disequilibrium (LD) whose frequencies may be associated with
environmental variables. The grasshopper “species complex”
Trimerotropis pallidipennis is considered to have several genetic
lineages distributed from North to South America in arid and semi-arid
high-altitude environments. The southernmost lineage, Trimerotropis sp.,
bears 4 to 7 putative inversion polymorphisms with clinal variation,
possibly allowing adaptation to temperate environments. We analyzed
chromosomal, mitochondrial and genome-wide SNP markers in 19
Trimerotropis sp. populations mainly distributed along two altitudinal
gradients (MS and Ju). We show that populations across Argentina are
formed by two main chromosomally and genetically differentiated
lineages: one distributed in 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,
genomic architecture analysis revealed four clusters of loci in high LD
that correspond to inversions, of which at least one is associated to a
chromosomal rearrangement, confirming its status as “true inversion”.
We demonstrated the stability of chromosome polymorphisms for more than
20 generations and the occurrence of non-neutral markers associated with
inversions and environmental variables. Inversion clines could be the
consequence of coupling between extrinsic postzygotic barriers, leading
to a hybrid zone, and spatially varying selection along environmental
gradients. These results provide a framework for future investigations
about candidate genes implicated in the rapid adaptation to new
environments.