An ontogenetic perspective on individual differences

Abstract

Phenotypic differences among individuals can arise during any stage of life. Although several distinct processes underlying individual differences have been defined and studied (e.g. parental effects, senescence), we lack an explicit, unified perspective for understanding how these processes contribute separately and synergistically to observed variation in functional traits. We propose a conceptual framework based on a developmental view of life-history variation, linking each ontogenetic stage with the types of individual differences originating during that period. In our view, the salient differences among these types are encapsulated by three key criteria: timing of onset, when fitness consequences are realized, and potential for reversibility. To fill a critical gap in this framework, we formulate a new term to refer to individual differences generated during adulthood-reversible state effects. We define these as 'reversible changes in a functional trait resulting from life-history trade-offs during adulthood that affect fitness', highlighting how the adult phenotype can be repeatedly altered in response to environmental variation. Defining individual differences in terms of trade-offs allows explicit predictions regarding when and where fitness consequences should be expected. Moreover, viewing individual differences in a developmental context highlights how different processes can work in concert to shape phenotype and fitness, and lays a foundation for research linking individual differences to ecological and evolutionary theory.

Keywords: carry-over effects; developmental effects; life-history trade-offs; phenotypic plasticity; reversible state effects; senescence.

Figure 1.

The contribution of an individual's experience to observed population variation at a single time point. Time is indicated on the x-axis, starting with conception (C); A₁ = the cessation of development, followed by successive points in adulthood (A₂–A₄). The y-axis indicates variation in a single functional trait. At conception (C), the trait varies by virtue of a number of genotypes in the population. Coloured lines represent 10 individuals with the same genotype, and subsequent intra-individual changes in the trait. By adulthood (A₁), trait variation has increased through different experiences in development, which is further influenced by experiences in adulthood. Other genotypes (C) result in similar diversification with regard to the trait (not shown). Thus, interpretation of population variation at a given point (frequency distribution at A₃) requires consideration of individual histories and all possible sources of individual differences. Note that the pattern of trait diversification in previous and later cohorts will temporally overlap with the cohort shown.

Figure 2.

An ontogenetic perspective on individual variation. Types of individual differences (on right) are specific to the life-history stage (in blue) in which they originate. Most types of individual differences can cause either immediate fitness effects or delayed fitness effects (e.g. carry-over effects).

Figure 3.

The cost of reproduction and its potential consequences for high- and low-quality individuals. Br, breeding season; NB, non-breeding season. The y-axis indicates individual state, in terms of condition relevant to breeding and survival. The unshaded area indicates condition sufficient for successful breeding. The light blue area indicates condition insufficient for breeding. The darker blue area indicates condition insufficient for survival. A high-quality individual (purple line) may experience energetic costs of a breeding attempt, but retain or regain sufficient condition during the non-breeding season, and thus incur no reversible state effect. A low-quality individual, however, may experience similar breeding costs (Br₁) but fail to return to sufficient breeding condition the following year (Br₂). This individual may skip the following breeding opportunity (green line) but return to breeding condition in the third year (Br₃); in this case, the reversible state effect is a missed breeding opportunity (Br₂). Alternatively, a low-quality individual may attempt to breed in insufficient condition (blue line) and suffer a reduced chance of survival; in this case, the reversible state effect is poor breeding condition, leading to death during the subsequent non-breeding season (NB₂).