Chromosomal inversions as drivers of ecological adaptation and
diversification in a grasshopper species complex
Abstract
The study of inversion polymorphisms along environmental gradients has
long attracted the attention of evolutionary biologists. Currently, the
application of genomic approaches has provided new evidences about the
role that these rearrangements might have played as drivers of
ecological adaptation and speciation. The grasshopper Trimerotropis
pallidipennis is considered a “species complex” composed of several
genetic lineages distributed from North to South America in arid and
semi-arid high-altitude environments. The southernmost lineage,
Trimerotropis sp., bears inversion polymorphisms whose frequencies vary
along environmental gradients. These polymorphisms may have allowed this
grasshopper to adapt to more temperate environments. Herewith, we
analyze chromosomal, mitochondrial and genome-wide SNP markers in 19
populations of Trimerotropis sp. mainly distributed along two
altitudinal gradients. We show that populations across Argentina are
formed by two main chromosomally 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, footprints of
secondary contact between divergent populations were detected, probably
leading to incipient speciation through selective disadvantages of
heterozygous individuals and asymmetrical gene flow. We demonstrated the
stability of inversion polymorphisms for more than 30 generations and
the occurrence of non-neutral markers associated with environmental and
chromosomal gradients. These results confirm the adaptive nature of the
chromosomal gradients and provide a framework to future investigations
about candidate genes that may be implicated in the rapid adaptation to
new environments.