Predator-induced allometric changes in the tail spine length of Daphnia: a distinct resource allocation strategy

Understanding resource allocation strategies underlying inducible defense is a challenging scientific issue, because of the difficulty in measuring resource allocations of defensive traits. We examined allometric changes to evaluate resource allocation strategies on the tail spine of Daphnia within and between species and further explore the allometric changes at different developmental stages and their relationship with growth and reproduction. We found that four Daphnia species (Daphnia magna, Daphnia sinensis, Daphnia galeata and Daphnia mitsukuri) can perform significant inducible defensive responses when exposed to fish kairomone. Different from the other Daphnia species, D. mitsukuri significantly enhanced the allometric slope of its tail spine when exposed to fish kairomone. We also found that allometric changes among different D. mitsukuri clones are significant in adult individuals. Furthermore, the allometric changes show a significant negative interaction with individual growth, indicating that a trade-off may exist between the resource allocations of tail spine elongation and growth. This study highlights the species-specific allometric changes in tail spine elongation and provides an explanation for this from resource allocations.

Anti-predation Defense Traits of Daphnia are Associated With the Gut Microbiota Composition Shaped by Fish Kairomone

Background: Gut microbiota plays an important role in host physiology and fitness. The gut microbiota can promote host health by influencing life history traits, especially in arthropods. However, it is not clear whether the performance of host defense traits in response to predator pressure in natural food webs is related to their gut microbiota composition. In this study, we used Daphnia magna as a model organism to investigate the relationship of D. magna life history traits and gut microbiota alterations under predator kairomone based on 16S rRNA amplicon sequencing.Result: We showed that the microbiota composition of D. magna was significantly affected by their predator risk and development stage. The relative abundance of Comamonadaceae (mainly Limnohabitans sp.) significantly decreased in the presence of predator kairomone. Furthermore, the presence of predator kairomone significantly reduced the α diversity of gut microbiota in D. magna with the increase of instar. Among them, the OTUs belonged to Epsilonbacteraeota and Firmicutes in the presence of predator kairomone were significantly higher than those in the control group. The results of functional predictions showed that predation pressure promote the metabolic function of gut microbiota, such as metabolism of energy, cofactors, and vitamins. By analyzing the correlation between the induced defense traits of D. magna and the relative abundance of bacteria, we found that the increased abundance of Comamonadaceae, Moraxellaceae, and Flavobacteriaceae were linearly correlated with the partial defense traits of D. magna. Specifically speaking, body size was positively correlated with an increased abundance of Comamonadaceae, whereas spine length was negatively correlated with an increased abundance of Comamonadaceae but was positively correlated with increased Flavobacteriaceae abundance. Conclusions: Our results suggested that predation risk can affect the composition of the gut microbiota in D. magna, which may indirectly induce the production of defensive traits in D. magna. The results of this study revealed an important role of gut microbiota in the development of defensive traits of Daphnia in response to fish predators. The correlation between microbial abundance and defense traits is of great significance for further understanding the effect of host-microbiota interaction on individual anti-predation defense.

Genomic regions associated with adaptation to predation in Daphnia often include members of expanded gene families

Predation has been a major driver of the evolution of prey species, which consequently develop antipredator adaptations. However, little is known about the genetic basis underpinning the adaptation of prey to intensive predation. Here, we describe a high-quality chromosome-level genome assembly (approx. 145 Mb, scaffold N50 11.45 Mb) of Daphnia mitsukuri , a primary forage for many fish species. Transcriptional profiling of D. mitsukuri exposed to fish kairomone revealed that this cladoceran responds to predation risk through regulating activities of Wnt signalling, cuticle pattern formation, cell cycle regulation and anti-apoptosis pathways. Genes differentially expressed in response to predation risk are more likely to be members of expanded families. Our results suggest that expansions of multiple gene families associated with chemoreception and vision allow Daphnia to enhance detection of predation risk, and that expansions of those associated with detoxification and cuticle formation allow Daphnia to mount an efficient response to perceived predation risk. This study increases our understanding of the molecular basis of prey defences, being important evolutionary adaptations playing a stabilizing role in community dynamics.

The impact of diel vertical migration on fatty acid patterns and allocation in Daphnia magna

In freshwater zooplankton diel vertical migration (DVM) is a widespread predator-avoidance behavior that is induced by kairomones released from fish. Thereby zooplankton reduces predation by fish by staying in deep and dark colder strata during daytime and migrating into warmer layers during night, and thus experiences diel alterations in temperature. Constantly lower temperatures have been shown to increase the relative abundance of polyunsaturated fatty acids (PUFAs) in Daphnia sp. Furthermore, a low dietary supply of the ω3-PUFA eicosapentaenoic acid (EPA) has been shown to limit the induction of DVM in Daphnia magna and the performance of D. magna under fluctuating temperatures, as experienced during DVM. In nature DVM of D. magna in response to fish is accompanied by the presence of fish-borne kairomone and diel fluctuations of depth dependent-parameters like temperature, food, and oxygen supply. Here we investigated the effect of factors, which are differing between Daphnia that perform DVM and those which do not. We selected to examine the effect of changing temperature and light conditions and of the presence/absence of fish kairomones on D. magna. For this purpose, we conducted a full factorial experimental design in which we grew D. magna under constantly warm temperatures in a diel light-dark regime or under alternating temperatures in darkness crossed with the presence or absence of fish kairomones. We analyzed the fatty acid composition of mature animals and of their offspring in each treatment. Simulation of the light and temperature regime of migrating animals in presence of the fish kairomone resulted in an increased relative allocation of the ω3-PUFA EPA, from adult animals to their offspring, manifesting as decreased EPA concentrations in mothers and increased EPA concentrations in their offspring in response to simulated DVM (mothers). Additionally, EPA concentrations in the offspring were affected by the interaction of simulated DVM and the fish cue. The presence of the fish kairomone alone increased the EPA concentration in the offspring, that was not experiencing simulated DVM. These findings lead to the conclusion that the temperature and light regime associated with DVM alone, as well as in combination with the DVM-inducing fish kairomones, alter the allocation of fatty acids to the offspring in a manner, which is beneficial for the offspring under the decreased average temperatures, which migrating animals are exposed to. A low dietary supply of ω3-PUFAs may constrain D. magna’s amplitude of DVM, but our results suggest that the next generation of animals may be capable of regaining the full DVM amplitude due to the effect of the fish kairomone and the experienced temperature fluctuations (and darkness) on tissue fatty acid composition. These findings suggest that fatty acid limitation in DVM performing Daphnia may be more severe for the maternal than for the offspring generation.

Transcriptional response to kairomone exposure in Daphnia magna: A candidate gene approach

Background: Daphnia (Brachiopoda, Cladocera) is a well-studied model organism providing unparalleled opportunity to test epigenetic regulation of predator avoidance mechanisms in aquatic ecosystems. The discovery of regulatory functions for microRNA molecules and recently described miRNA profiles of Daphnia make it an ideal system to probe for posttranslational regulatory mechanisms mediated by kairomone released by predatory fish. However, despite a number of studies that focused on mRNA transcript level differences, no miRNA studies associated with kairomone exposure have been reported. Results: Exposing D. magna to fish kairomone from birth to the first reproduction was found to result in the differential expression of the four miRNAs tested: miR-7, miR-34, miR-317, and miR-375. Normalized transcript levels for each miRNA were found to vary across the exposure period with no clear conserved pattern of expression despite functional target analyses by GO, COG and KEGG indicating that predicted miRNA target genes are likely involved in related biological activities. Analysis of six mRNA transcripts (Hsp70, Hsp90, actin, AKT, GYS and IGFR), identified in previous studies as kairomone-mediated genes in Daphnia magna, were also carried out. Similar to that obtained for miRNAs, the mRNA transcript levels showed varying degrees of temporal regulation across the exposure time course with the two heat shock transcripts exhibiting elevated levels at early and late time points of kairomone exposure while the AKT, GYS, and IGFR transcripts had an general decrease in expression during the first 96 hours. Conclusions: Differential mRNA expression data supports the premise of an ecological trade-off between the cost of general biological processes and that of survival under long-term kairomone stress. Transcript levels for the four miRNAs tested were found to vary across developmental time with kairomone exposure which suggests that they may have a role in regulating morphological, behavioral or physiological responses by altering target gene expression. These studies lay the foundation for future work aimed at linking miRNAs and their target transcripts to changes in the signaling events that govern Daphnia response to kairomone specific stress.