Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population

Abstract

Although the pedigree-based inbreeding coefficient F predicts the expected proportion of an individual's genome that is identical-by-descent (IBD), heterozygosity at genetic markers captures Mendelian sampling variation and thereby provides an estimate of realized IBD. Realized IBD should hence explain more variation in fitness than their pedigree-based expectations, but how many markers are required to achieve this in practice remains poorly understood. We use extensive pedigree and life-history data from an island population of song sparrows ( Melospiza melodia ) to show that the number of genetic markers and pedigree depth affected the explanatory power of heterozygosity and F , respectively, but that heterozygosity measured at 160 microsatellites did not explain more variation in fitness than F . This is in contrast with other studies that found heterozygosity based on far fewer markers to explain more variation in fitness than F . Thus, the relative performance of marker- and pedigree-based estimates of IBD depends on the quality of the pedigree, the number, variability and location of the markers employed, and the species-specific recombination landscape, and expectations based on detailed and deep pedigrees remain valuable until we can routinely afford genotyping hundreds of phenotyped wild individuals of genetic non-model species for thousands of genetic markers.

Recent advances in conservation and population genomics data analysis

“…Genomic approaches capture variation in realized inbreeding that is missed by pedigree analysis due to the stochastic effects of linkage and unknown common ancestors of parents (Franklin, 1977; Thompson, 2013). Thus, while deep and accurate pedigrees can often precisely measure individual inbreeding in species with many chromosomes and/or high recombination rates (Kardos et al., 2018; Knief, Kempenaers, & Forstmeier, 2017; Nietlisbach et al., 2017), genomic approaches are expected to more reliably measure inbreeding and inbreeding depression (Kardos, Luikart, & Allendorf, 2015a; Kardos et al., 2018; Keller, Visscher, & Goddard, 2011; Wang, 2016). Given that many studies have used only shallow pedigrees or few DNA markers, it is possible that power to detect inbreeding depression has been low; therefore, inbreeding depression could be more common, widespread, and severe than previously thought.…”

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

“…Hansson & Westerberg, ; Rodriguez‐Quilon et al ., ), and the associated question of the link between marker‐based heterozygosity and inbreeding coefficients (e.g. Balloux et al ., ; Berenos et al ., ; Nietlisbach et al ., ), although these models are not mutually exclusive. A third mechanism, ‘direct effects’, was applicable to older study techniques such as allozymes (e.g.…”

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population

“…However, comparisons of observed relatedness among mates with that expected given random mating revealed little evidence of active inbreeding avoidance through nonrandom social pairing (Keller and Arcese 1998;Reid et al 2006) or through nonrandom extrapair reproduction (Reid et al 2015a(Reid et al , 2015b. This is despite evidence of strong inbreeding depression in fitness (Keller 1998;Reid et al 2014;Nietlisbach et al 2017). Further, female extrapair reproduction is heritable (Reid et al 2011b), but females receive no obvious direct benefits (e.g., nuptial gifts, offspring provisioning) from extrapair males, and extrapair reproduction can reduce offspring fitness Sardell et al 2012).…”

“…We first compiled a social pedigree linking all banded offspring to their observed mother and her socially paired male spanning 1975-2015 (Reid et al 2014(Reid et al , 2015a(Reid et al , 2015b. Since 1993, all adults and banded offspring were blood sampled and genotyped at ∼160 highly polymorphic microsatellite loci, and all offspring were assigned to genetic sires with 199% individual-level statistical confidence (Nietlisbach et al 2015(Nietlisbach et al , 2017Reid et al 2015a). We then compiled a genetic pedigree linking all banded offspring to their mother and true genetic father (Sardell et al 2010;Reid et al 2014Reid et al , 2015aReid et al , 2015bNietlisbach et al 2015).…”