Individuals’ expected genetic contributions to future generations, reproductive value, and short-term metrics of fitness in free-living song sparrows (Melospiza melodia)

Abstract

Appropriately defining and enumerating “fitness” is fundamental to explaining and predicting evolutionary dynamics. Yet, general theoretical concepts of fitness are often hard to translate into quantities that can be measured in wild populations experiencing complex environmental, demographic, genetic, and selective variation. Although the “fittest” entities might be widely understood to be those that ultimately leave most descendants at some future time, such long‐term legacies can rarely be measured, impeding evaluation of the degree to which tractable short‐term metrics of individual fitness could potentially serve as useful direct proxies. One opportunity for conceptual and empirical convergence stems from the principle of individual reproductive value ( V i ), here defined as the number of copies of each of an individual's alleles that is expected to be present in future generations given the individual's realized pedigree of descendants. As V i tightly predicts an individual's longer term genetic contribution, quantifying V i provides a tractable route to quantifying what, to date, has been an abstract theoretical fitness concept. We used complete pedigree data from free‐living song sparrows ( Melospiza melodia ) to demonstrate that individuals’ expected genetic contributions stabilize within an observed 20‐year (i.e. approximately eight generation) time period, allowing estimation of individual V i . Considerable among‐individual variation in V i was evident in both sexes. Standard metrics of individual lifetime fitness, comprising lifespan, lifetime reproductive success, and projected growth rate, typically explained less than half the variation. We thereby elucidate the degree to which fitness metrics observed on individuals concur with measures of longer term genetic contributions and consider the degree to which analyses of pedigree structure could provide useful complementary insights into evolutionary outcomes.

Fitness Estimation for Ecological Studies: An Evaluation in Columbian Ground Squirrels

“…Other methods for estimating fitness are not directly applicable to the problem of comparing trait forms in empirical research, but may hold promise for future improvements. Perhaps the most attractive is the use of offspring from a pedigree, perhaps even including both male and female relatives (Brommer et al, 2004;Reid et al, 2019). An alternative to our use of changes in population size to adjust for environmental variation might involve fitness measures that take demographic and environmental stochasticity into account (e.g., Benton and Grant, 2000;Engen et al, 2009;Saether and Engen, 2015).…”

“…The frequencies of trait groups change over time when natural selection occurs. Thus, rather than the number of offspring or even grand-offspring for measuring changes due to natural selection (Brommer et al, 2004;Reid et al, 2019), the most useful measure is the growth rate of trait forms or associations of trait forms among generations. The most commonly used measure of increase in trait forms is lifetime reproductive success (e.g., Clutton-Brock, 1988;Grafen, 1988;Merilä and Sheldon, 2000;Jensen et al, 2004;Descamps et al, 2006;McLoughlin et al, 2007).…”

“…The lack of strong association of the relative indices of individual fitness and lifetime reproductive success indicate that the widespread use of lifetime reproductive success as a fitness measure might have to be reconsidered. On the other hand, both individual fitness and lifetime reproductive success were equally moderate predictors of the number of maternal gene copies passed on to future generations in collared flycatchers and Ural owls (respectively, Ficedula albicollis, Strix uralensis; Brommer et al, 2004), and in a study that included both male and female gene copies in song sparrows Reid et al, 2019). These studies were conducted, however, without obvious evidence of selection favoring particular traits.…”

“…Lifetime reproductive success is not sensitive to the timing of successful reproductive events (that might occur at any point in a lifecycle), but individual fitness measures are sensitive to when such events occur (Brommer et al, 2002). The impact of this difference on studies of natural selection is currently unknown (Brommer et al, 2004;Reid et al, 2019).…”

The Price equation and reproductive value

“…One formal treatment of anticipating reproductive value is by Barton & Etheridge [22], but their assumptions, specifically of weak selection, reduce the impact of multiple counting. A recent empirical paper by Reid et al [23] considers how to measure fitness in a field study with enough long-term data to incorporate anticipation if desired.…”