Little parallelism in genomic signatures of local adaptation in two sympatric, cryptic sister species

Species living in sympatry and sharing a similar niche often express parallel phenotypes as a response to similar selection pressures. The degree of parallelism within underlying genomic levels is often unexplored, but can give insight into the mechanisms of natural selection and adaptation. Here, we use multi-dimensional genomic associations to assess the basis of local and climate adaptation in two sympatric, cryptic Crematogaster levior ant species along a climate gradient. Additionally, we investigate the genomic basis of chemical communication in both species. Communication in insects is mainly mediated by cuticular hydrocarbons (CHCs), which also protect against water loss and, hence, are subject to changes via environmental acclimation or adaptation. The combination of environmental and chemical association analyses based on genome-wide Pool-Seq data allowed us to identify single nucleotide polymorphisms (SNPs) associated with climate and with chemical differences. Within species, CHC changes as a response to climate seem to be driven by phenotypic plasticity, since there is no overlap between climate- and CHC-associated SNPs. The only exception is the odorant receptor OR22c, which may be a candidate for population-specific CHC recognition in one of the species. Within both species, climate is significantly correlated with CHC differences, as well as to allele frequency differences. However, associated candidate SNPs, genes and functions are largely species-specific and we find evidence for minimal parallel evolution only on the level of genomic regions (J = 0.04). This highlights that even closely related species may follow divergent evolutionary trajectories when expressing similar adaptive phenotypes.

Automated summary

Species living in sympatry and sharing a similar niche often exhibit parallel phenotypes in response to similar selection pressures, with unexplored levels of parallelism at the genomic level providing insight into natural selection and adaptation mechanisms. Through multi-dimensional genomic associations, the study identified the genetic basis of local and climate adaptation in two sympatric ant species, as well as the genomic basis of chemical communication. Despite significant correlations between climate and CHC differences within species, candidate SNPs, genes, and functions associated with these traits were largely species-specific, highlighting minimal parallel evolution even in closely related species expressing similar adaptive phenotypes.