Maternal consumption of non‐toxic Microcystis by Daphnia magna induces tolerance to toxic Microcystis in offspring

Abstract

1. Freshwater cyanobacterial blooms are a worldwide environmental issue. These blooms often comprise both non-toxic and toxic species and strains. Populations of some zooplankton, including Daphnia, have been shown to adapt locally to toxic Microcystis through maternal effects. However, Microcystis populations vary spatially and temporally in the absolute and relative abundances of non-toxic and toxic genotypes. 2. We examined variation in induction of tolerance to toxic cyanobacteria in offspring from two Daphnia magna clones (JS and AH) fed diets containing Scenedesmus by itself or in combination with either a non-toxic or a toxic clone of Microcystis aeruginosa. The diets containing Microcystis included relatively more cyanobacteria within each week of the 3 week experiment (week 1-10%, week 2-20%, week 3-40%). Daphnia neonates were collected from these three treatments at the end of the third week and fed a diet containing Scenedesmus and toxic Microcystis for 3 weeks before a suite of lifehistory, physiological and biochemical measurements were made on the surviving animals. 3. Neonates from mothers fed toxic and non-toxic Microcystis showed enhanced growth and reproduction compared to neonates produced from mothers fed only Scenedesmus. Our results showed that Daphnia neonates could be induced to tolerate toxic cyanobacteria when their mothers were fed diets containing non-toxic or toxic strains of cyanobacteria. Furthermore, elevated RNA-DNA ratios, superoxide dismutase activity and catalase activity in neonates fed diets containing non-toxic or toxic Microcystis clones suggested that the mechanisms behind these changes involved processes associated with metabolism and antioxidation. 4. Our study shows that non-toxic cyanobacteria can induce tolerance to toxic cyanobacteria and further elucidates the general importance of maternal effects on tolerance of cyanobacteria in herbivorous zooplankton.

Individual variation in plasticity dulls transgenerational responses to stress

“…For instance, Beyer and Hambright () 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, ). 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, ).…”

“…One potential explanation for the lack of treatment differences in the second experimental generation is that maternal exposure to cyanobacteria did not influence the phenotypes of offspring. This deserves consideration as most prior studies have used toxic Microcystis to test for the presence of transgenerational plasticity (Beyer & Hambright, ; Gustafsson et al, ; Jiang et al, ; Lyu et al, ; Peng et al, ; Zhu et al, ). Here, we used a non‐toxic strain of Anabaena which may influence the extent to which Daphnia respond across generations (Walsh et al, ).…”

“…However, the role of phenotypic plasticity, including transgenerational plasticity, in the process of adaptation remains unclear. 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, ).…”

“…Such negative consequences of cyanobacteria during development can have maladaptive effects on subsequent generations (Beyer & Hambright, ; Zhu et al, ). However, adaptive transgenerational responses can also be present in populations and may counteract or even outweigh the influence of maladaptive effects (Lyu et al, ; Schwarzenberger & Von Elert, ). Given these contrasting sets of results, we evaluated transgenerational responses to cyanobacteria across a large number of clones.…”

Transcriptomic analysis dissects the mechanistic insight into the Daphnia clonal variation in tolerance to toxic Microcystis

“…Of note, the uniform understanding of this negative relation between cyanobacterial and zooplankton abundance has been questioned in some lab‐ and field‐scale investigations (Gustafsson et al ; Sarnelle and Wilson ; Jiang et al ; Lyu et al ), revealing that Daphnia had the ability to gain tolerance to dietary toxic Microcysits . The reproductive success of Daphnia is characterized by cyclical parthenogenesis, which is involved in alternation between sexual reproduction and parthenogenesis.…”