Timing of maternal exposure to toxic cyanobacteria and offspring fitness in Daphnia magna: Implications for the evolution of anticipatory maternal effects

Abstract

Organisms that regularly encounter stressful environments are expected to use cues to develop an appropriate phenotype. Water fleas (Daphnia spp.) are exposed to toxic cyanobacteria during seasonal algal blooms, which reduce growth and reproductive investment. Because generation time is typically shorter than the exposure to cyanobacteria, maternal effects provide information about the local conditions subsequent generations will experience. Here, we evaluate if maternal effects in response to microcystin, a toxin produced by cyanobacteria, represent an inheritance system evolved to transmit information in Daphnia magna. We exposed mothers as juveniles and/or as adults, and tested the offspring's fitness in toxic and non‐toxic environments. Maternal exposure until reproduction reduced offspring fitness, both in the presence and in the absence of toxic cyanobacteria. However, this effect was accompanied by a small positive fitness effect, relative to offspring from unexposed mothers, in the presence of toxic cyanobacteria. This effect was mainly elicited in response to maternal exposure to toxic cyanobacteria early in life and less so during reproduction. None of these effects were explained by changes in egg size. A meta‐analysis using our and others’ experiments suggests that the adaptive value of maternal effects to cyanobacteria exposure is weak at best. We suggest that the beneficial maternal effect in our study is an example of phenotypic accommodation spanning generations, rather than a mechanism evolved to transmit information about cyanobacteria presence between generations.

The jury is still out regarding the generality of adaptive ‘transgenerational’ effects

“…2a-d); (2) effects were stronger when ancestors were exposed during embryonic development (Fig. 2g), which supports recent findings in water fleas (Radersma et al, 2018).…”

Temperature elevation reduces the sensitivity of invasive cladoceran Daphnia lumholtzi to filamentous cyanobacterium Raphidiopsis raciborskii

“…We also recorded three cases, only in R+ 20°C treatment, wherein neonates were unable to leave the brood chamber, leading to their death. Although a plethora of consequences of the presence of cyanobacteria are known for reproduction‐related traits in daphnids (Claska & Gilbert ; Bednarska & Slusarczyk, ; Radersma, Hegg, Noble, & Uller, ), our study is the first to demonstrate neonates becoming trapped in the brood chambers of experimental animals in response to exposure to cyanobacterial filaments and a lower temperature. As few cases were observed in this study, this phenomenon appears to be quite rare in daphnids.…”

Individual variation in plasticity dulls transgenerational responses to stress

“…Conversely, other reports have shown that the effects of cyanobacteria will be ameliorated over time via adaptive transgenerational responses that enhance herbivore performance and fitness (Gustafsson et al, ; Jiang et al, ; Lyu et al, ; Peng et al, ; Schwarzenberger & Von Elert, ). One potential explanation for inconsistency among studies is that all prior studies assayed a small number of clones (but see Radersma et al, ). This is important because our present study assayed a large number of Daphnia clones and revealed extensive genetic variation in within‐ and across‐generation responses to cyanobacteria (Table , Figure ).…”

“…Transgenerational phenotypic plasticity is hypothesized to play a significant role in the long-term ecological consequences of anthropogenic change, including cyanobacterial blooms (Gustafsson et al, 2005;Salinas & Munch, 2012;Sultan et al, 2009). On the one hand, several studies suggest that prolonged exposure to cyanobacteria will have a compounding negative influence on the fitness of subsequent generations (Beyer & Hambright, 2017;Faassen et al, 2015;Radersma et al, 2018;Zhu et al, 2015). For instance, Beyer and Hambright (2017) found that rotifers whose mothers were exposed to a toxic cyanobacteria (Microcystis) exhibited reduced survival and fecundity, regardless of their own food environment (Beyer & Hambright, 2017).…”

“…For instance, several studies have discovered evidence for adaptive transgenerational responses (e.g., physiological, morphological) to cyanobacteria that could ameliorate negative fitness consequences over time (Gustafsson, Rengefors, & Hansson, ; Jiang et al, ; Lyu et al, ; Peng et al, ; Schwarzenberger & Von Elert, ). Yet, other reports highlight that maternal stress from cyanobacteria generates maladaptive effects (e.g., reduced growth, survival) in offspring, which could have a compounding negative influence on the fitness of subsequent generations (Faassen, García‐Altares, Mendes e Mello, & Lürling, ; Radersma, Hegg, Noble, & Uller, ; Zhu et al, ).…”