Parental effects in ecology and evolution: mechanisms, processes and implications

Abstract

As is the case with any metaphor, parental effects mean different things to different biologists--from developmental induction of novel phenotypic variation to an evolved adaptation, and from epigenetic transference of essential developmental resources to a stage of inheritance and ecological succession. Such a diversity of perspectives illustrates the composite nature of parental effects that, depending on the stage of their expression and whether they are considered a pattern or a process, combine the elements of developmental induction, homeostasis, natural selection, epigenetic inheritance and historical persistence. Here, we suggest that by emphasizing the complexity of causes and influences in developmental systems and by making explicit the links between development, natural selection and inheritance, the study of parental effects enables deeper understanding of developmental dynamics of life cycles and provides a unique opportunity to explicitly integrate development and evolution. We highlight these perspectives by placing parental effects in a wider evolutionary framework and suggest that far from being only an evolved static outcome of natural selection, a distinct channel of transmission between parents and offspring, or a statistical abstraction, parental effects on development enable evolution by natural selection by reliably transferring developmental resources needed to reconstruct, maintain and modify genetically inherited components of the phenotype. The view of parental effects as an essential and dynamic part of an evolutionary continuum unifies mechanisms behind the origination, modification and historical persistence of organismal form and function, and thus brings us closer to a more realistic understanding of life's complexity and diversity.

Figure 1

Conceptual illustration of continuity of phenotype and information between developmental stages (columns; germ cells (GC), embryo stage and adult stage) and generations (rows). Each developmental stage is a subject to selection pressure (S_{germ cells}, natural selection during GC stage; S_embryo, selection during embryo stage; S_adult, selection during adult stage). Developmental offset between generations results in similar selection pressures (black rectangle shows similar selection on function (adult stage), development (embryo stage) and germ cell induction (germ cell stage) in three overlapping generations). Black single-headed solid arrows show induction of germ cells from embryonic tissues, and red dashed arrows show epigenetic effects typically classified as parental effects. Solid grey lines indicate individual development. The figure also illustrates the concept of phenotype-specific effects (integration of dashed red and solid black arrows) on various developmental stages and the corresponding accumulation, retention and transmission of functionally important phenotypic modifications through parental effects. Overlap between developmental stages (e.g. germ cells and embryo) will result in the overlap of paths of parental effects. Transference of adaptive function mostly involves late ontogeny somatic tissue transmissions, while the importance of genetic inheritance decreases with ontogenetic decrease in the predictability of parentally transferred resources. Path I is parental effects on germ cells (including germ cell-to-germ cell and somatic tissue-to-germ cell effects), and path II shows somatic tissue-to-germ cell effects. Path III—somatic tissue-to-somatic issue effects on offspring development, including templating and priming parental effects, and path IV includes somatic tissue-to-somatic tissue parental effects on offspring growth and development, including provisioning, sexual imprinting, learning and inheritance of parental ecological and social environments (see text for examples of parental effects for each path). Adapted from Badyaev (2008).