Abstract
Understanding the evolutionary dynamics of inbreeding and inbreeding depression requires unbiased estimation of inbreeding depression across diverse mating systems. However, studies estimating inbreeding depression often measure inbreeding with error, for example, based on pedigree data derived from observed parental behavior that ignore paternity error stemming from multiple mating. Such paternity error causes error in estimated coefficients of inbreeding (f) and reproductive success and could bias estimates of inbreeding depression. We used complete "apparent" pedigree data compiled from observed parental behavior and analogous "actual" pedigree data comprising genetic parentage to quantify effects of paternity error stemming from extra-pair reproduction on estimates of f, reproductive success, and inbreeding depression in free-living song sparrows (Melospiza melodia). Paternity error caused widespread error in estimates of f and male reproductive success, causing inbreeding depression in male and female annual and lifetime reproductive success and juvenile male survival to be substantially underestimated. Conversely, inbreeding depression in adult male survival tended to be overestimated when paternity error was ignored. Pedigree error stemming from extra-pair reproduction therefore caused substantial and divergent bias in estimates of inbreeding depression that could bias tests of evolutionary theories regarding inbreeding and inbreeding depression and their links to variation in mating system.
Highlights
Numerous studies have shown that, in normally outbreeding organisms, inbred offspring resulting from matings among relatives are typically less fit than outbred offspring resulting from matings among non-relatives (e.g., Wright 1977; Keller and Waller 2002; Charlesworth and Willis 2009)
We show that inbreeding depression in key fitness components was substantially underestimated due to pedigree error stemming from extra-pair paternity, and report a case of reverse attenuation where paternity error caused inbreeding depression to be overestimated
Actual f and apparent f were moderately correlated across all 1808 juveniles (overall correlation coefficient: r = 0.64; linear regression coefficient: b = 0.60 ± 0.02, R2 = 0.41, Fig. 1A; r = 0.67 and 0.62 for females and males separately). This relationship was weak (r = 0.18, b = 0.14 ± 0.04 [SE], R2 = 0.03, Fig. 1A) across 492 individuals that had been sired by an extra-pair male, and much stronger (r = 0.83, b = 0.82 ± 0.02 [SE], R2 = 0.68, Fig. 1A) across 1316 individuals that had been sired by their apparent father
Summary
Numerous studies have shown that, in normally outbreeding organisms, inbred offspring resulting from matings among relatives are typically less fit than outbred offspring resulting from matings among non-relatives (e.g., Wright 1977; Keller and Waller 2002; Charlesworth and Willis 2009). Such reduced fitness, termed “inbreeding depression”, is often postulated to cause selection against inbreeding and thereby to shape dispersal and mating system evolution Such pedigree errors, which will cause error in estimates of f and potentially bias estimates of inbreeding depression, may be normal rather than exceptional, in wild population studies
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