Microsatellites reveal heterosis in red deer

Abstract

The ¢tness consequences of inbreeding and outbreeding are poorly understood in natural populations. We explore two microsatellite-based variables, individual heterozygosity (likely to correlate with recent inbreeding) and a new individual-speci¢c internal distance measure, mean d 2 (focusing on events deeper in the pedigree), in relation to two measures of ¢tness expressed early in life, birth weight and neonatal survival, in 670 red deer calves (Cervus elaphus) born on the Isle of Rum between 1982 and 1996. For comparison, we also analyse inbreeding coe¤cients derived from pedigrees in which paternity was inferred by molecular methods.Only 14 out of 231 calves (6.1%) had non-zero inbreeding coe¤cients, and neither inbreeding coe¤cient nor individual heterozygosity was consistently related to birth weight or neonatal survival. However, mean d 2 was consistently related to both ¢tness measures. Low mean d 2 was associated with low birth weight, especially following cold Aprils, in which foetal growth is reduced. Low mean d 2 was also associated with low neonatal survival, but this e¡ect was probably mediated by birth weight because ¢tting birth weight to the neonatal survival model displaced mean d 2 as an explanatory variable. We conclude that in the deer population ¢tness measures expressed early in life do not show evidence of inbreeding depression, but they do show evidence of heterosis, possibly as a result of population mixing. We also demonstrate the practical problems of estimating inbreeding via pedigrees compared with a direct marker-based estimate of individual heterozygosity. We suggest that, together, individual heterozygosity and mean d 2 , estimated using microsatellites, are useful tools for exploring inbreeding and outbreeding in natural populations.

Heterozygosity and lungworm burden in harbour seals (Phoca vitulina)

“…The publication of the measure mean d-squared, an estimator of microsatellite allele similarity, and the demonstration that it predicts aspects of fitness in deer and seals (Coltman et al, 1998;Coulson et al, 1998) stimulated renewed interest in the link between heterozygosity and fitness (David, 1998). Subsequent studies have developed both new and more effective measures for estimating heterozygosity (Coltman et al, 1999;Amos et al, 2001;Aparicio et al, 2006) and confirmed that panels of as few as 10 presumed neutral microsatellite markers often reveal statistically significant correlations with fitness.…”

Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus)

“…IR reflects the relatedness of the parents of an individual by determining the degree of allele-sharing relative to random expectations across all loci (Amos et al 2001). Standardized mean d 2 (hereafter referred to as d 2 ) is a measure focused on events deeper in the pedigree than individual heterozygosity (Hedrick et al 2001) and is based on the genetic distance between parental gamete genomes (Coulson et al 1998(Coulson et al , 1999. d 2 was calculated for each individual as the squared distance in repeat units between two alleles at a given locus, averaged over all loci typed for that individual (Coulson et al 1999) and then standardized by dividing each value by the maximum observed at that locus (Hedrick et al 2001).…”

“…Molecular metrics are commonly used as a surrogate for pedigree inbreeding coefficients (f), because the latter can be logistically difficult to obtain within natural populations. The most frequently used molecular metrics of heterozygosity in HFCs analyses include standardized multilocus heterozygosity (stMLH; Coltman et al 1999), internal relatedness (IR; Amos et al 2001) and standardized mean d 2 (Coulson et al 1998). However, it has been suggested that the correlation between molecular heterozygosity and pedigree inbreeding coefficients is too weak to be of biological significance (Coltman and Slate 2003;Balloux et al 2004;Slate et al 2004;Hansson and Westerberg 2008).…”

Heterozygosity–fitness correlations in blue tit nestlings (Cyanistis caeruleus) under contrasting rearing conditions

“…In most cases, the negative effects of inbreeding (or the positive effects of outbreeding) have been found more often among females than males. The differences in the effects of heterozygosity or inbreeding between males and females may be explained by sex-specific gene expression (Yun and Agrawal 2014), maternal investments (Charpentier et al 2006), food acquisition (Charpentier et al 2006), growth strategies (Coulson et al 1998), sexual selection pressure and life history (Ebel and Phillips 2016).…”