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

Abstract

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.

Parallel genomic responses to historical climate change and high elevation in East Asian songbirds

“…This result probably mirrors hemoglobin adaptation in HA birds: While occasional cases of parallel evolution at particular hemoglobin amino acid substitutions have been observed ( 56 ), more generally, derived hemoglobin proteins in HA birds have parallel functions that are the result of distinct molecular evolutionary solutions ( 7 , 50 , 57 ). Such genetic nonparallelism has been regarded to be probably caused by the low levels of heterozygosity of replicated species ( 15 – 17 ). Our comparisons do not show increased genic parallelism across the three widespread parids with higher heterozygosity compared with the four HA endemics.…”

“…Theoretical studies suggest that these inconsistent adaptive solutions may be influenced by differences in standing genetic variation (i.e., heterozygosity) ( 13 , 14 ). A loss of heterozygosity within small populations might reduce opportunities for parallel evolution across replicated species by decreasing the probability that the same alleles are available in response to shared selection pressures ( 15 – 17 ).…”

Capturing the rapidly evolving study of adaptation

“…Results such as those found in Hartke et al.’s (2021) and Zueva et al.’s (2021) work highlight that replicated adaptive evolution can be due to largely nonparallel changes at the genetic level. Other recent studies have similarly documented limited parallelism at the genetic level despite substantial parallelism at the organismal or phenotypic level (e.g.…”

“…Interestingly, Hartke et al. (2021) show that although these ant species are exposed to the same environmental selection pressures, genetic variation associated with local climate adaptation is largely nonparallel.…”

“…Thus, tests for parallel local adaptation to climatic selection pressures of closely related insect species in sympatry (e.g. Hartke et al., 2021) can be useful in this context. Such studies of parallel evolution often address the general issue of the determinism of evolutionary change by testing whether similar adaptive outcomes at the organismal or phenotypic level depend on similar underlying genomic variation.…”