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

Jane M Reid,Peter Arcese,Lukas F Keller,Pirmin Nietlisbach,Matthew E Wolak

doi:10.1002/evl3.118

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.

Highlights

Defining and enumerating “fitness” is fundamental to explaining and predicting evolutionary dynamics
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
The correlations rp between the genetic contributions expected after 20 years and in each preceding year exceeded 0.95 by 12–13 years posthatch in both sexes, and were typically close to one by the basic theoretical expectation of ß15 years posthatch (Fig. 3)

Summary

Introduction

Defining and enumerating “fitness” is fundamental to explaining and predicting evolutionary dynamics. The “fittest” entities might be widely understood to be those that 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. 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 Vi. Considerable among-individual variation in Vi was evident in both sexes. Biologists have rarely directly evaluated individuals’ longer term genetic contributions, or evaluated the degree to which an individual’s own reproductive output, which is somewhat easier to measure, adequately predicts its longer term contribution and could provide a reliable proxy indicator

Methods

Results

Conclusion