Experimental evidence of rapid heritable adaptation in the absence of initial standing genetic variation

The success of genetically depauperate populations in the face of environmental change is contrary to the expectation that high genetic diversity is required for rapid adaptation. Alternative pathways such as environmentally induced genetic modifications and non-genetic heritable phenotypes have been proposed mechanisms for heritable adaptation within an ecologically relevant timeframe. However, experimental evidence is currently lacking to establish if, and to what extent, these sources of phenotypic variation can produce a response.

To test if adaptation can rapidly occur in the absence of initial standing genetic variation and recombination in small populations, we (i) exposed replicate monoclonal populations of the microzooplankton Brachionus calyciflorus to a culturing regime that selected for phenotypic variants with elevated population growth with either high or low phosphorus food for a period of 55 days and (ii) examined population-level response in two fully factorial common garden experiments at day 15 and 35 of the exposure experiment.

Within six generations, we observed heritable local adaptation to nutrient limitation. More specifically, populations with a history of exposure to P-limited food exhibited higher population growth rates under low P food conditions than populations with a high P exposure history. However, the capacity for such a response was found to vary among clones.

Our study finds that although standing genetic variation is considered essential for rapid heritable adaptation, the rapid emergence of de novo genetic variation or alternative sources of phenotypic variation could aid in the establishment and persistence of low diversity populations.

Methods
The goal of this study was to experimentally test if adaptation can occur in the absence of initial standing genetic variation and recombination in small populations within an ecologically relevant time frame. To investigate this question, we conducted a two-part experiment using two genotypes of the microzooplankton Brachionus calyciflorus. In the first part of the experiment (further referred to as the ‘exposure experiment’), we exposed replicate monoclonal populations to a culturing regime selecting for phenotypic variants with elevated population growth rates for at least 20 generations with either high (HP) or low (LP) phosphorus food. LP food has a C:P content that deviates strongly from the requirements for growth in B. calyciflorus, and thus represents low-quality food in comparison to HP food (Sterner & Hessen, 1994; Zhou & Declerck, 2019). In the second part of the experiment, we performed two full factorial common garden experiments at two successive time points, using individuals isolated from the exposure experiment.

Population growth rate was the response variable in both the exposure and common garden experiments. Population growth rate was calculated on a daily basis as (lnNt-lnN0)/t, where N0 and Nt represent the population size at the start and end of each 24-h period, and t the duration of the period in days.