Gene expression in closely-related species mirrors local adaptation: Consequences for responses to a warming world

Background/Question/Methods

Climate change is likely to influence species’ distributions by enhancing some populations, diminishing others, and enabling establishment in new areas. The details of these influences will depend on species’ interactions and, notably, evolutionary histories. In particular, species with reduced gene flow are more likely to be composed of populations adapted to their local environments, and when dispersal is limiting, these locally adapted species may be diminished by climate change widely across their range.

Our group previously demonstrated local adaptation to temperature in populations of Erynnis propertius, a butterfly native to the western United States with limited dispersal capability. In Papilio zelicaon--a butterfly with higher gene flow and dispersal capability that shares large portions of its range with E. propertius--we found no evidence for local adaptation but also no evidence that populations from cooler regions will benefit from warming.

To explain the factors potentially underlying these responses, we investigated the molecular and genetic makeup of these species by characterizing their mRNA in de-novo transcriptome sequencing. This alternative to genome sequencing allowed us to comprehensively measure gene expression for individuals from sample populations under different temperature regimes in a common-garden experiment, mirroring that used to study local adaptation at the phenotypic level.

Results/Conclusions

We found many genes for both species that were differentially expressed between source populations independent of temperature treatment indicating widespread population differentiation at the molecular level. These simple population differences may be explained by drift or other factors, though gene annotation suggests that several of these differentiated genes are involved in host-plant detoxification. For E. propertius, we found evidence of localization in gene expression (genes differentially regulated by populations in different ways in response to climate change), corresponding to the previously identified local adaptation. Localized genes appear to be involved in metabolism and oxidative stress. In contrast, P. zelicaon showed no locally tuned genes, again supporting previous phenotypic results. These findings highlight the importance of considering local adaptation in the context of climate change, as well as the utility of transcriptomics to investigate functional population differences in non-model species. Understanding population differences is crucial to generating realistic predictions of species’ responses to climate change.