Maternal effects in the model system Daphnia: the ecological past meets the epigenetic future

Abstract

Maternal effects have been shown to play influential roles in many evolutionary and ecological processes. However, understanding how environmental stimuli induce within-generation responses that transverse across generations remains elusive, particularly when attempting to segregate confounding effects from offspring genotypes. This review synthesizes literature regarding resource- and predation-driven maternal effects in the model system Daphnia, detailing how the maternal generation responds to the environmental stimuli and the maternal effects seen in the offspring generation(s). Our goal is to demonstrate the value of Daphnia as a model system by showing how general principles of maternal effects emerge from studies on this system. By integrating the results across different types of biotic drivers of maternal effects, we identified broadly applicable shared characteristics: 1. Many, but not all, maternal effects involve offspring size, influencing resistance to starvation, infection, predation, and toxins. 2. Maternal effects manifest more strongly when the offspring's environment is poor. 3. Strong within-generation responses are typically associated with strong across-generation responses. 4. The timing of the maternal stress matters and can raise or lower the magnitude of the effect on the offspring's phenotype. 5. Embryonic exposure effects could be mistaken for maternal effects. We outline questions to prioritize for future research and discuss the possibilities for integration of ecologically relevant studies of maternal effects in natural populations with the molecular mechanisms that make them possible, specifically by addressing genetic variation and incorporating information on epigenetics. These small crustaceans can unravel how and why non-genetic information gets passed to future generations.

Fig. 1. Photograph of an adult female Daphnia pulex.

Daphnia are freshwater, filter feeding microcrustaceans belonging to the superorder Cladocera. The large black circle in the head region is a compound eye. The digestive tract can be easily seen via the bright green color of consumed algae. The multicellular, elongated ovoids within the brood chamber located toward the posterior of the animal are parthenogenetic embryos. Photograph taken by Trenton C. Agrelius with the ventral side to the left and head is oriented to the top.

Fig. 2. Diagram of the cyclically parthenogenetic life cycle common to most Daphnia.

In the field, multiple parthenogenetic (asexual) generations usually occur before a single generation of sexual reproduction. Reproductive modes seasonally switch in response to environmental changes, such as temperature changes or food scarcity. Parthenogenetically produced eggs develop immediately and are carried in the brood chamber until their release as neonates. In contrast, sexual reproduction involves fertilized eggs that are encapsulated in a structure known as an ephippium and enter dormancy. Under laboratory conditions, clonal lines can be maintained through continuous asexual reproduction.

Fig. 3. Schematic detailing the environmental attributes reviewed, the effects commonly observed, and results on offspring phenotypes.

Maternal exposure is linked to changes in gene expression, provisioning, and enzymatic alterations that ultimately affect offspring egg size. Egg size and provisioning dictate key life history traits like age and size at maturation and clutch size. Dashed arrows represent potential interactions.

Fig. 4. Diagram showing when a maternal effect can be expected based on the timing of exposure during development.

Arrows on top refer to the maternal generation (G₀), arrows on bottom to the embryonic/offspring generation (G₁). Solid blue arrows indicate when the environmental exposure results in an unambiguous maternal effect for the first clutch (C₁) of G₀ offspring; the dotted blue arrow indicates when an unambiguous maternal effect is less likely because packaging in oogenesis has already begun. Since maternal provisioning occurs during oogenesis, maternal exposure to environmental stimuli at the dotted blue arrow is less likely to alter the phenotypic outcomes of C₁ embryos in a meaningful way but could result in potential provisioning differences for C₂ offspring (eggs housed in the brood chamber are not supplied with materials by the mother after extrusion). The solid black arrow indicates the point at which some aspects of the environment may directly affect the phenotype of offspring from the first eggs produced by G₀, rendering purported maternal effects ambiguous. Solid orange and violet arrows indicate exposure times for an unambiguous maternal effect in C₂ and C₃, respectively. Green arrows show where exposure of the offspring generation (G₁) can result in an unambiguous maternal effect for the first clutch produced in the subsequent generation.