Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes

Abstract

Organisms producing resting stages provide unique opportunities for reconstructing the genetic history of natural populations. Diapausing seeds and eggs often are preserved in large numbers, representing entire populations captured in an evolutionary inert state for decades and even centuries. Starting from a natural resting egg bank of the waterflea Daphnia, we compare the evolutionary rates of change in an adaptive quantitative trait with those in selectively neutral DNA markers, thus effectively testing whether the observed genetic changes in the quantitative trait are driven by natural selection. The population studied experienced variable and well documented levels of fish predation over the past 30 years and shows correlated genetic changes in phototactic behavior, a predator-avoidance trait that is related to diel vertical migration. The changes mainly involve an increased plasticity response upon exposure to predator kairomone, the direction of the changes being in agreement with the hypothesis of adaptive evolution. Genetic differentiation through time was an order of magnitude higher for the studied behavioral trait than for neutral markers (DNA microsatellites), providing strong evidence that natural selection was the driving force behind the observed, rapid, evolutionary changes.

Figure 1

(Left) Changes in resting egg flux and density of stocked fish in Oud Heverlee Pond during a period of 26 years after its creation (1970–1996). Fish stock densities for each year were obtained from the owners of the pond (16) and aligned with the sediment record of ephippia abundance assuming a constant rate of sediment accumulation through time, corrected for compaction. The right (depth) axis applies to core 1. (Right) Average length (±2 SE) of resting egg cases isolated from three successive core sections. (Inset) Our definition of dorsal rim length as an index of egg size.

Figure 2

Phototactic behavior (mean ± 2 SE) of 10 clones from each of the three main periods in fish-stocking history [bottom (1970–1972), low predation; middle (1976–1979), high predation; top (ca. 1988), reduced predation] in the absence (open symbols) and presence (solid symbols) of fish kairomone. Within each subpopulation, the clones are ordered according to increasing values of phototactic index in the absence of fish kairomone.

Figure 3

Vertical profiles of allele frequencies for three microsatellite loci (Dma3/2, Dma11, and Dma12) as determined directly from resting eggs isolated from seven successive sediment depths.

Figure 4

Comparison of measures of genetic differentiation among three D. magna subpopulations separated in time. Q_ST values refer to phototactic behavior: Q_ST(1), phototactic behavior in absence of fish kairomone: Q_ST(2), phototactic behavior in presence of fish kairomone; Q_ST(3), change in behavior upon exposure to fish kairomone. G_ST values refer to microsatellite markers: G_ST(1), hatched populations; G_ST(2), resting eggs. Confidence intervals around Q_ST values were obtained by bootstrapping; confidence intervals around G_ST values were calculated from values obtained for the different loci studied.