The importance of intraspecific variation in zooplankton for adaptive insurance in aquatic ecosystems

Background/Question/Methods

Climate can result in unexpected intraspecific responses because environmental change can have direct effects on phenotypes through selection, as well as indirect effects through food webs interactions. Moreover, unpredictable climate fluctuations can present a moving target for phenotype matches for optimising population fitness, sometimes resulting in (mal)adaptation. Our objectives were: 1) evaluate the importance of migration and environmental selection from climatic micro-gradients for population trait (mal)adaptation at local and regional scales, and 2) quantify the relative influence of climate-driven environmental change on intraspecific traits from abiotic variables and from food web processes. We focused on phenotypic and genomic responses in a dominant calanoid copepod across a series of shallow, freshwater ponds. We employed an experiment and whole-genome sequencing to detect signatures of selection in relation to the climatic and pH variables in local pond populations, and to quantify the relative level of gene flow between ponds. We used a metapopulation model to evaluate the influence of migration on (mal)adaptation between ponds with divergent selection at the regional scale. We measured population-level differences in body size, fecundity, and essential fatty acids, and used structural equation modelling to evaluate the relative importance of microclimatic gradients and food webs on the traits.

Results/Conclusions

Genomic data revealed signatures of local adaptation to microclimatic and environmental gradients (pH, temperature) in the presence of high gene flow among ponds. Experimental data revealed that (mal)adaptative acid tolerance was maintained within certain pond populations, likely from high migration and gene flow between the spatially proximate ponds with divergent selection. However, at a regional scale, metapopulation models showed that migration reduced maladaptation across populations. Climate-driven temperature fluctuations resulted in unexpected positive relationships between temperature, copepod DHA content and body size, which positively related with fecundity. The previously unrecognised positive effect of temperature on body size was mediated by indirect effects through the food web via the phytoplankton community and brook trout in warm ponds that likely stimulated phytoplankton resources through enhanced nutrient cycling. Overall, our findings underscore the under-recognized importance of 1) migration and intraspecific variation, that can include maladaptive phenotype-environment mismatch, for adaptive insurance in face of environmental unpredictability at the regional scale, and 2) indirect food web interactions in mediating local intraspecific responses of key aquatic species to climate change. The findings that we present are especially relevant for small, shallow bodies of water that commonly occur across north-temperate and Arctic landscapes undergoing rapid climate change.