Abstract The adaptive nature of phenotypic plasticity is widely documented in natural populations. However, little is known about the evolutionary forces that shape genetic variation in plasticity within populations. Here we empirically address this issue by testing the hypothesis that stabilizing selection shapes genetic variation in the anti-predator developmental plasticity of Daphnia pulex . The anti-predator morphological defense is characterized by pedestal and spikes that grow on the back of the Daphnia neck following exposure to predator cure. We characterized variation in this plasticity using a novel, high-throughput phenotyping method that describes the entire dorsal shape amongst >100 D. pulex strains originating from a natural population in the UK. We found low genetic diversity for morphological defenses among genetically diverse clones upon predation risk exposure. The strongest reduction in genetic variation was observed in areas of greatest phenotypic plasticity, which we interpret as evidence of stabilizing selection. By assessing among-clone variance in clonally related, field derived strains, we contrasted mutational variation (V m ) to standing variation (V g ). We found that V g /V m is lowest in areas of greatest plasticity. These data strongly suggest that stabilizing selection operates directly on phenotypic plasticity, providing a rare glimpse into the evolution of fitness related traits in natural populations.
Ecological genomics aims to understand the functional association between environmental gradients and the genes underlying adaptive traits. Many genes that are identified by genome-wide screening in ecologically relevant species lack functional annotations. Although gene functions can be inferred from sequence homology, such approaches have limited power. Here, we introduce ecological regulatory genomics by presenting an ontology-free gene prioritization method. Specifically, our method combines transcriptome profiling with high-throughput cis-regulatory sequence analysis in the water fleas Daphnia pulex and Daphnia magna. It screens coexpressed genes for overrepresented DNA motifs that serve as transcription factor binding sites, thereby providing insight into conserved transcription factors and gene regulatory networks shaping the expression profile. We first validated our method, called Daphnia-cisTarget, on a D. pulex heat shock data set, which revealed a network driven by the heat shock factor. Next, we performed RNA-Seq in D. magna exposed to the cyanobacterium Microcystis aeruginosa. Daphnia-cisTarget identified coregulated gene networks that associate with the moulting cycle and potentially regulate life history changes in growth rate and age at maturity. These networks are predicted to be regulated by evolutionary conserved transcription factors such as the homologues of Drosophila Shavenbaby and Grainyhead, nuclear receptors, and a GATA family member. In conclusion, our approach allows prioritising candidate genes in Daphnia without bias towards prior knowledge about functional gene annotation and represents an important step towards exploring the molecular mechanisms of ecological responses in organisms with poorly annotated genomes.
ROS (reactive oxygen species) as well as components of the antioxidant redox systems may act as signals. To link acute environmental change with gene expression, changes in ROS and GSH/GSSG (reduced/oxidized glutathione) level were measured upon acute changes in temperature or oxygen availability in the aquatic key species Daphnia magna together with HIF-1 (hypoxia-inducible factor 1)-mediated Hb (haemoglobin) expression.Acute exposures to 30°C or hypoxia, which induced tissue hypoxia (and possibly elevated mitochondrial ROS production), caused resembling fluctuations of ROS and GSH levels, with frequency and number of peaks increasing and their delay decreasing with the magnitude of environmental change (size of tissue hypoxia). Acute hyperoxia induced an initial decrease in ROS level. Evidence is also provided for the promoting effects of ROS on catalase activity. A signalling function of the ROS fluctuations upon acute changes in temperature was found in the case of Hb, the expression of which is known to respond to temperature changes, by detecting corresponding time courses of both transcription and protein formation.ROS-dependent signalling was affected by changes in temperature or oxygen availability. Feedback interactions between ROS and the glutathione redox system, possibly driven by elevated mitochondrial ROS production, likely contributed to the appearance of the ROS and GSH fluctuations upon acute environmental change. Fluctuating ROS levels, which reflect for the magnitude of environmental change, could be a way to transfer information on ROS production to subsequent processes (gene expression) while avoiding too-high and damaging ROS levels.
Abstract Species across the tree of life can switch between asexual and sexual reproduction. In facultatively sexual species, the ability to switch between reproductive modes is often environmentally dependent and subject to local adaptation. However, the ecological and evolutionary factors that influence the maintenance and turnover of polymorphism associated with facultative sex remain unclear. To address this basic question, we studied the ecological and evolutionary dynamics of polymorphism in reproductive strategy in a metapopulation of the model facultative sexual, Daphnia pulex , located in the southern United Kingdom. We found that patterns of clonal diversity, but not genetic diversity varied with ephemerality. Reconstruction of a multi-year pedigree demonstrated the co-existence of clones that were found to differ in their investment into male production. Mapping of quantitative variation in male production using lab-generated and field-collected individuals identified multiple putative QTL underlying this trait, and we identified a plausible candidate gene. The evolutionary history of these QTL suggests that they are relatively young, and male limitation in this system is a rapidly evolving trait. Our work highlights the dynamic nature of the genetic structure and composition of facultative sex across space and time and suggests that quantitative genetic variation in reproductive strategy can undergo rapid evolutionary turnover.
Knowledge of the molecular basis of phenotypic responses to environmental cues is key to understanding the process of adaptation. Insights to adaptation at an evolutionary time scale can be gained by observing organismal responses before and after a shift in environmental conditions, but such observations can rarely be made. Using the ecological and genomic model Daphnia, we linked transcriptomic responses and phosphorus (P)-related phenotypic traits under high and low P availability. We mapped weighted gene coexpression networks to traits previously assessed in resurrected ancient (600 years old) and modern Daphnia pulicaria from a lake with a historic shift in P-enrichment. Subsequently, we assessed evolutionary conservation or divergence in transcriptional networks of the same isolates. We discovered highly preserved gene networks shared between ancient genotypes and their modern descendants, but also detected clear evidence of transcriptional divergence between these evolutionarily separated genotypes. Our study highlights that phenotypic evolution is a result of molecular fine-tuning on different layers ranging from basic cellular responses to higher order phenotypes. In a broader context, these findings advance our understanding how populations are able to persist throughout major environmental shifts.
All animals and plants respond to changes in the environment during their life cycle. This flexibility is known as phenotypic plasticity and allows organisms to cope with variable environments. A common source of environmental variation is predation risk, which describes the likelihood of being attacked and killed by a predator. Some species can respond to the level of predation risk by producing morphological defences against predation. A classic example is the production of pedestals and head spikes in the water flea, Daphnia pulex, which defend against predation from Chaoborus midge larvae. Previous studies of these defences have focussed on changes in pedestal size and the number of spikes along a gradient of predation risk. Although these studies have provided a model for continuous plasticity, they do not capture the whole-organism shape response to predation risk. In contrast, studies in fish and amphibians focus on shape as a complex, multi-faceted trait made up of different variables. In this study, we analyse how multiple aspects of shape change in D. pulex along a gradient of predation risk from C. flavicans. These changes are dominated by the inducible morphological defence, but there are also changes in the size and shape of the head and the body. We detected change in specific modules of the body plan and a level of integration among modules. These results are indicative of a complex, multi-faceted response to predation and provide insight into how predation risk drives variation in shape and size at the level of the whole organism.
A key challenge for ecological and ecotoxicological risk assessment is to predict the risk of organisms when exposed simultaneously to multiple stressors in sub-lethal concentrations. Here, we assessed whether sub-lethal concentrations of an anthropogenic stressors, the heavy metal copper (Cu), mediates the impacts of a natural ecological threat to species, predation risk, among six distinct Daphnia pulex clones. We investigated the interaction between the two stressors on morphological defenses and on several life-history traits including maturation time, size at maturity, somatic growth rate and survival rates. Combining a life table experiment on a response surface design, we found no evidence that the heavy metal copper mediates the effects of predator cue induced morphological responses in the tested D. pulex clones. However, our data indicate that copper can mediate several key life-history responses to predation risk. For age at maturity, we found also clear evidence that the observed interaction between predation risk and copper varied by whether clones were strong or weak morphological responders. Specific exploration of the relationship between morphological responses and life history traits under predation risk and copper suggest a strong hypothesis for multiple strategies to deal with multiple stressors. While interactions between different stressors make it harder to predict their outcomes, and ultimately assess water quality regulations about the effects of such stressors, our study provides evidence that life history theory can aid in understanding and predicting their impacts.
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