Adapting to an increasingly stressful environment: Experimental evidence for ‘micro-evolutionary priming’

In many natural systems animal populations are exposed to increasing levels of stress. Stress levels tend to fluctuate and long-term increases in average stress levels are often accompanied by greater amplitudes of such fluctuations. Micro-evolutionary adaptation may allow populations to cope with gradually increasing stress levels but may not prevent their extirpation during acute stress events unless adaptation to low stress levels also increases their tolerance to acute stress.

We tested this idea, here called ‘micro-evolutionary priming’, by exposing populations of the monogonont rotifer species Brachionus calyciflorus to four levels of copper stress (control, low, intermediate and high) during a multigenerational selection experiment. Subsequently, in a common garden experiment we exposed randomly selected subsets of genotypes (clones) of each of these populations to low, intermediate and high copper levels and assessed their population growth performance across multiple generations.

Compared to populations with an exposure history to copper, genotypes of control populations suffered strong growth reductions when exposed to intermediate and high levels of copper, mainly as the result of high mortality rates. Remarkably, when exposed to low copper levels, fitness differences between genotypes of control populations and populations adapted to these low levels were very small, whereas the latter strongly outperformed the first at intermediate and high copper levels.

These results highlight the potentially strong but hitherto largely ignored impact of micro-evolutionary priming on the performance of populations in a changing environment. We discuss potential consequences of micro-evolutionary priming for the persistence of populations and the spatial eco-evolutionary dynamics of metapopulations.

Methods
We conducted a selection experiment followed by a common garden experiment. In the selection experiment, we exposed 6 genetically identical populations of the freshwater monogonont rotifer Brachionus calyciflorus s.s.to two treatments, i.e. a copper addition treatment and a copper free control treatment. All populations underwent six cycles (Cycles 1 to 6); during each cycle clonal population growth was followed by sexual reproduction and the formation of dormant propagules. Dormant propagules produced during each cycle were stored and partly used to start up the next cycle. In the copper addition treatment, copper levels were stepwise increased at the beginning of each cycle (from 30, 45, 50, 55, 57.5, 60 to 62.5 µg Cu/L in Cycles 1 to 6, respectively).

For the common garden experiment, we established two clonal lines from dormant propagules for each population at the end of Cycles 2, 4 and 6. Populations of all clonal lines were subjected to concentrations of 45, 57.5 and 62.5 µg Cu/L (corresponding with Cycles 2, 4 and 6, respectively). After an acclimation phase, demographic variables of experimental populations were monitored for 5 days.

A reduced version of the common garden experiment was repeated to verify if actual Cu concentrations equaled targeted concentrations in each treatment.