Individual variation in plasticity dulls transgenerational responses to stress

Abstract

Much research has shown that environmental stress can induce adaptive and maladaptive phenotypic changes in organisms that persist for multiple generations. Such transgenerational phenotypic plasticity shrouds our understanding of the long‐term consequences of ongoing anthropogenic pressures. Here, we evaluated within‐ and transgenerational phenotypic responses to food stress in the freshwater crustacean, Daphnia. We reared 45 clones of Daphnia pulicaria each on high‐quality Scenedesmus and low‐quality (but also non‐toxic) cyanobacteria (generation 1). Offspring produced by generation 1 adults were then reared on Scenedesmus (generation 2), and life‐history traits were measured across both generations. The results show that Daphnia in generation 1 exhibited reduced fitness (i.e., delayed maturation, lower reproductive output, increased clutch interval) when reared in the presence of cyanobacteria as opposed to high‐quality food. However, maternal stress had no clear influence on the fitness of offspring. That is, Daphnia in the second experimental generation had similar mean trait values, irrespective of whether their mothers were reared on cyanobacteria or high‐quality food. Signals of transgenerational life‐history effects were obscured, in part, by extensive clonal variation among Daphnia in the direction of transgenerational responses to cyanobacteria (i.e., adaptive and maladaptive plasticity). Further analyses demonstrated that such individual variance in plasticity might be open to selection and potentially offer a means of contemporary adaptation to cyanobacteria. Taken together, our results denote a link between the overall strength of transgenerational responses to the environment and the potential for rapid evolution in populations. A free Plain Language Summary can be found within the Supporting Information of this article.

Transgenerational plasticity in the eye size of Daphnia

“…Daphnia that were fed a diet containing cyanobacteria in generation 1 produced a smaller eye than Daphnia fed green algae (figure 1). Given that we fed Daphnia a non-toxic strain of cyanobacteria, the production of a smaller eye in generation 1 likely stems from the reduced nutritional content of Anabaena versus Scenedesmus [67]. We examined whether the smaller eye size produced on the cyanobacteria diet in generation 1 is due to a fitness trade-off with some other trait.…”

“…We tested for an influence of cyanobacteria on the eye size of Daphnia using clones from two lakes in Wisconsin, USA (Allequash, Mendota). The experiments that generated the images that we used to assess eye size are published [67]. Here we provide a summary of the protocols.…”

“…To test for clonal variation in plasticity, we included the clone × food × generation interaction as a random effect. We also tested for trade-offs between investment in eye size and life-history traits using the published data [67] by performing multiple regressions with eye size entered as the dependent variable, life-history trait (age at maturation, clutch size) and length entered as the independent variables. We performed these regressions separately for each generation [69].…”

“…Here we tested the influence of cyanobacteria on transgenerational plasticity in eye size. We reared 45 clones of Daphnia pulicaria in the presence and absence of cyanobacteria ( Anabaena ) and evaluated variation in relative eye size in the parental and offspring generations [67]. If exposure to cyanobacteria results in a trade-off between investment in life history versus eye tissue, then we expect to observe a decline in relative eye size and the production of smaller eyes will continue in the offspring generation.…”

Mitigating Elemental Imbalance

“…This aspect of B. calyciflorus' life history offers the additional benefit that genetically distinct lines can easily be produced and compared. Although previous investigations of de novo heritable variation have taken advantage of apomictic reproduction in other zooplankton species (e.g., Gillis & Walsh, 2019;Kielland et al 2017;Walsh et al 2015), the short generation time of B. calyciflorus (Declerck & Papakostas, 2017;Stelzer, 2017) provides the added advantage that many generations can be studied over a relatively short period.…”