Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows

L.F Keller,J.M Reid,P Arcese

doi:10.1098/rspb.2007.0961

Abstract

Mutation accumulation (MA) and antagonistic pleiotropy (AP) have each been hypothesized to explain the evolution of ‘senescence’ or deteriorating fitness in old age. These hypotheses make contrasting predictions concerning age dependence in inbreeding depression in traits that show senescence. Inbreeding depression is predicted to increase with age under MA but not under AP, suggesting one empirical means by which the two can be distinguished. We use pedigree and life-history data from free-living song sparrows (Melospiza melodia) to test for additive and interactive effects of age and individual inbreeding coefficient (f) on fitness components, and thereby assess the evidence for MA. Annual reproductive success (ARS) and survival (and therefore reproductive value) declined in old age in both sexes, indicating senescence in this short-lived bird. ARS declined with f in both sexes and survival declined with f in males, indicating inbreeding depression in fitness. We observed a significant age×f interaction for male ARS (reflecting increased inbreeding depression as males aged), but not for female ARS or survival in either sex. These analyses therefore provide mixed support for MA. We discuss the strengths and limitations of such analyses and therefore the value of natural pedigreed populations in testing evolutionary models of senescence.

Highlights

The magnitude of the deleterious effect of inbreeding, known as inbreeding depression, is a key parameter in evolutionary and population biology (Charlesworth & Charlesworth 1987; Crnokrak & Roff 1999; Hedrick & Kalinowski 2000)
Precise knowledge of age-specific variation in fitness is critical to understanding life-history evolution and dynamics of age-structured populations (Charlesworth 1994; Coulson et al 2001; Altwegg et al 2007), and is the focus of considerable research (e.g. Forslund & Part 1995; Komdeur 1996; Newton & Rothery 1997; Nichols et al 1997; Loison et al 1999; Møller & de Lope 1999; McElligott et al 2002; Reid et al 2003; Velando et al 2006; Low et al 2007)
Of primary current interest, Annual reproductive success (ARS), survival and reproductive value all declined in old age in both sexes

Summary

Introduction

The magnitude of the deleterious effect of inbreeding, known as inbreeding depression, is a key parameter in evolutionary and population biology (Charlesworth & Charlesworth 1987; Crnokrak & Roff 1999; Hedrick & Kalinowski 2000). Recent studies have used laboratory populations of Drosophila melanogaster, Callosobruchus maculatus, Callosobruchus chinensis and Stator limbatus to test whether inbreeding depression in fitness components increases with age, as predicted under MA (Tanaka 1990; Charlesworth & Hughes 1996; Hughes et al 2002; Snoke & Promislow 2003; Fox et al 2006; Swindell & Bouzat 2006b).

Results

Conclusion