Natural Selection for Grazer Resistance to Toxic Cyanobacteria: Evolution of Phenotypic Plasticity?

Abstract

We studied the selection response of the freshwater grazing zooplankter, Daphnia galeata, to increased abundance of cyanobacteria in its environment. Cyanobacteria are a poor-quality and often toxic food. Distinct genotypes of D. galeata were hatched from diapausing eggs extracted from three time horizons in the sediments of Lake Constance, Europe, covering the period 1962 to 1997, a time of change in both the prevalence of planktonic cyanobacteria and levels of phosphorus pollution. We assessed whether the grazers evolved to become more resistant to dietary cyanobacteria by exposing genetically distinct clones to two diets, one composed only of the nutritious green alga, Scenedesmus obliquus (good food), and the other a mixture of S. obliquus and the toxic cyanobacterium Microcvstis aeruginosa (poor food). Genotype performance was measured as the specific rate of weight gain from neonate to maturity (gj). We evaluated evolutionary change in the Daphnia population using an analysis of reaction norms based on relative (log-transformed) changes in gj. Log(gj) is a measure of the proportional effect of dietary cyanobacteria on other fitness components of the Daphnia phenotype. For comparison, we also analyze absolute (i.e., nontransformed) changes in gj and discuss the interpretations of the two approaches. Statistical results using a general linear model demonstrate a significant effect of genotype (showing differences in gj among genotypes), a significant genotype x food-type interaction (showing differences in phenotypic plasticity among genotypes), and, in the case of log-transformed data, a significant sediment-genotype-age x food-type interaction. The latter shows that phenotypic plasticity evolved over the period studied. Two constraints act on response to selection in the D. galeata-Lake Constance system. First, gj on a diet containing poor food is highly correlated with gj on a diet of good food, thus evolving resistance also meant evolving an increase in gj on both diets. Second, because genotypes with a high gj also grow to a large adult body size, which in turn increases Daphnia vulnerability to fish predation, we suggest that selection only acted to favor genotypes possessing a high potential gj after cyanobacteria became prevalent. The presence of cyanobacteria depressed realized gj and led to animals of small adult body size even if their genotypes had the potential for high gj and large size. With realized gj reduced, genotypes with an inherently high value could be selected even in the presence of predatory fish. The joint action of selection by dietary cyanobacteria and vulnerability to fish predation provides an explanation for the observed evolution of resistance to poor food through reduced phenotypic plasticity.

Initial conditions mediate the interaction between Daphnia and bloom‐forming cyanobacteria

“…Lastly, the lack of congruence between field and laboratory results could be related to the recently documented ability of Daphnia to adapt to the presence of toxic cyanobacteria in their diet (Hairston et al 2001;Gustafsson and Hansson 2004;Sarnelle and Wilson 2005). Specifically, D. pulicaria genotypes isolated from lakes with abundant cyanobacteria are better able to grow on a diet of 100% toxic M. aeruginosa than genotypes from lakes with few cyanobacteria (Sarnelle and Wilson 2005).…”

“…All of the above suggest that dominance of a phytoplankton assemblage by cyanobacteria may interfere with the ability of Daphnia to suppress total phytoplankton biomass, as has been suggested many times (Sommer et al 1986;Benndorf and Henning 1989;Ghadouani et al 2003). Recent studies indicate that Daphnia may adapt to tolerate cyanobacteria in the diet (Hairston et al 2001;Gustafsson and Hansson 2004;Sarnelle and Wilson 2005), but the significance of these findings with respect to Daphnia control of cyanobacteria has yet to be determined.…”

Testing for resistance of pelagic marine copepods to a toxic dinoflagellate

“…Recently, it has been shown that the ecological relationship between zooplankton grazers and toxic algae is closely shaped by their evolutionary history (Hairston et al, 1999(Hairston et al, , 2002Colin and Dam, 2002a). Freshwater studies have shown that populations of Daphnia sp.…”

“…Freshwater studies have shown that populations of Daphnia sp. from lakes where toxic cyanobacteria have bloomed for generations have evolved resistance to the toxic algae (Gilbert, 1990;Hairston et al, 1999;Hairston et al, 2002). Resistance has enabled the Daphnia to feed and grow at higher rates in the presence of the toxic cyanobacteria than conspecifics never exposed to the toxic algae.…”

Ecological genomics in Daphnia: stress responses and environmental sex determination

“…Results demonstrated increased behavioral plasticity in response to predator kairomones, and order of magnitude higher genetic differentiation for the trait than for neutral markers, consistent with a strong role for selection as the driver of rapid, directional changes. Another example demonstrated evolution of resistance to toxic food sources (cyanobacteria) through a reduction in phenotypic plasticity over time (Hairston et al, 2001). In a similar way, combining molecular biology and genomics with paleolimnology may test hypotheses about adaptation in populations exposed to severe metal contamination (Pollard et al, 2003).…”