Gene-phenotype-environment associations: evidence for a role of natural selection?
Gene flow is thought to constrain divergence by swamping locally adapted alleles (but see ), and while phenotype-environment associations can indicate responses to natural selection , they may also reflect phenotypic plasticity and non-random dispersal . Evidence for selection is therefore strengthened when observed trait divergence has a genomic component (i.e., “gene-phenotype-environment” associations). Importantly, all traits we measured had substantial additive genetic variation, suggesting high levels of potential for traits to respond to selection. This was further reflected at the genomic level, where we were able to successfully recover similar genomic architecture as previously reported for this species. Using the mapped genomic architecture, we show that while divergence of most traits was not linked to a genomic component, relative spine lengths was. Specifically, genomic regions that were associated with pelvic spine length (that were longer in deeper waters), were divergent across water depth strengthening the conclusion that the observed divergence in pelvic spine length is a result of divergent natural selection – likely due to predation.
Mapping the causative pathways from genes to phenotypes is a notoriously challenging task , but identifying the genes on regions involved in gene-phenotype-environment associations provide insight into the molecular mechanisms underlying adaptation. On the genomic regions associated with the pelvic spine length - depth relationship, we found two genes (ULK2 and CCNB1) with haplotypes coding for alternate amino acids. These are functionally interesting as ULK2 is a serine/threonine kinase which, along with its homolog ULK1, interacts with the master regulator of metabolism (mTOR) and regulates apoptosis in response to starvation, and CCNB1 codes for Cyclin B1, a major kinase regulator which activates mitosis and regulates the dynamics of the cell cycle. Whilst these findings suggest candidate molecular functions underlying responses to natural selection, explicit follow up studies are needed to get at the causal relationships with pelvic spine length variation.
Many of the regions of the genome that were correlated with environmental variation in our study were not linked to observed trait divergence. This is not surprising given that we only measured a selected subset of traits within specific functional categories. An understanding of what biological functions these regions are associated with can therefore provide hypotheses about targets of divergent natural selection for future studies. In our study, the biological processes implicated in genomic regions included developmental processes, such as development of nervous and sensory systems. Notably, visual response to abiotic stimulus and perception of sound were enriched biological functions that were associated with the community structure of invertebrates. This is particularly interesting for Mývatn stickleback due to potential for influencing ability to respond to prey stimulus, and because the sensory drive hypothesis posits that an organisms’ communication system should be especially sensitive to ecological variation .
Although adaptation can occur across exceptionally short time frames , selection often acts multifariously and environments are rarely stable temporally, resulting in fluctuating selection pressures . Mývatn is a highly dynamic ecosystem, where multiple dimensions of its ecology and, importantly, stickleback population size fluctuate substantially through time . Our environmental, phenotypic and genomic data were collected at a single point in time, and may therefore not accurately reflect the selective environment experienced by Mývatn stickleback within or across generations. Whilst using ecological data collected at the same (single) time point as genomic and phenotypic data is common practice in studies that investigate selection in wild populations , tracking gene-phenotype-environment associations through time would allow inferences on how patterns of phenotypic and genomic variation withstand, or respond to, temporal fluctuations in selective pressures. In context of Mývatn stickleback, this would also facilitate the exploration of the spatiotemporal balance between adaptive divergence and gene flow.