The evolution of trait correlations constrains phenotypic adaptation to high CO2 in a eukaryotic alga

Microbes form the base of food webs and drive biogeochemical cycling. Predicting the effects of microbial evolution on global elemental cycles remains a significant challenge due to the sheer number of interacting environmental and trait combinations. Here we present an approach for modeling the interactive effects of de novo biological change and multivariate trait correlation evolution using principal component axes. We investigated the outcome of thousands of possible adaptive walks parameterized using empirical evolution data from the alga Chlamydomonas exposed to high CO2. We found that only a limited number of phenotypes emerged. Applying adaptive trait correlations to the starting population (historical bias) accelerated adaptation while highly convergent, nonrandom phenotypic solutions emerged irrespective of bias. These findings are consistent with a limited set of evolutionary trajectories underlying the vast amount of possible trait combinations (phenotypes). Critically, we demonstrate that these dynamics emerge in an empirically defined multidimensional trait space and show that trait correlations, in addition to trait values, must evolve to explain multi-trait adaptation. Identifying high probability high-fitness outcomes based on trait correlations is necessary in order to connect microbial evolutionary responses to biogeochemical cycling, thereby enabling the incorporation of these dynamics into global ecosystem models.