Consistent and flexible maternal effects: how the environments of a mother influence the offspring phenotype.

The environment experienced by a mother influences offspring phenotype through maternal effects, which can have significant adaptive benefits for both the mother and the offspring. However, the ways in which maternal environments influence offspring development are extremely diverse, and empirical studies using an outcome-based approach often fail to support different maternal effect hypotheses. We argue that this is in part because such studies overlook the ontogeny of the maternal phenotype. Here, we review how the environments experienced by a mother across different life stages influence the development of the maternal phenotype. Then, we propose a new framework that differentiates between two main processes of maternal effects according to the life stage at which a specific maternal trait is developed and how long its effect persists during the mother's reproductive life. The "consistent" maternal phenotype is developed mainly during a mother's early life and consistently affects the phenotype of all offspring produced during her lifetime, whereas the "flexible" maternal phenotype changes in response to environmental conditions experienced during her adult life and affects the phenotype of her subsequent offspring. We review how consistent and flexible maternal effects can contribute to different maternal effect processes, such as condition-transfer effects, cascading effects, intergenerational plasticity and developmental programming. We also provide empiricists with a quantitative genetic method, which integrates the ontogenetic scope into maternal effect testing, to determine how the early or late environments shape the maternal phenotype across ontogeny and then examine how this maternal phenotype affects offspring phenotype. We highlight that this conceptual and methodological framework of disassembling the multiple processes by which genes and environments interactively influence the maternal and offspring phenotypes will help us to explain the astonishing variation in maternal strategies and life-history trade-off patterns.