Elevated Heterozygosity in Adults Relative to Juveniles Provides Evidence of Viability Selection on Eagles and Falcons

Abstract

Viability selection yields adult populations that are more genetically variable than those of juveniles, producing a positive correlation between heterozygosity and survival. Viability selection could be the result of decreased heterozygosity across many loci in inbred individuals and a subsequent decrease in survivorship resulting from the expression of the deleterious alleles. Alternatively, locus-specific differences in genetic variability between adults and juveniles may be driven by forms of balancing selection, including heterozygote advantage, frequency-dependent selection, or selection across temporal and spatial scales. We use a pooled-sequencing approach to compare genome-wide and locus-specific genetic variability between 74 golden eagle (Aquila chrysaetos), 62 imperial eagle (Aquila heliaca), and 69 prairie falcon (Falco mexicanus) juveniles and adults. Although genome-wide genetic variability is comparable between juvenile and adult golden eagles and prairie falcons, imperial eagle adults are significantly more heterozygous than juveniles. This evidence of viability selection may stem from a relatively smaller imperial eagle effective population size and potentially greater genetic load. We additionally identify ~2000 single-nucleotide polymorphisms across the 3 species with extreme differences in heterozygosity between juveniles and adults. Many of these markers are associated with genes implicated in immune function or olfaction. These loci represent potential targets for studies of how heterozygote advantage, frequency-dependent selection, and selection over spatial and temporal scales influence survivorship in avian species. Overall, our genome-wide data extend previous studies that used allozyme or microsatellite markers and indicate that viability selection may be a more common evolutionary phenomenon than often appreciated.

Exploiting genomic synteny in Felidae: cross-species genome alignments and SNV discovery can aid conservation management

“…Poolseq can be used to provide a high-quality approach for genotyping the collective genomic profile of a population, comparable to population-level allele frequency estimates of individual WGS [ 63 ]. Poolseq is a cost-effective method for assessing population structure and genome-wide patterns of variation [ 64 , 65 ], but does present statistical challenges in deriving estimates of demographic and other inferences that rely on individual heterozygosity. Estimating allele frequencies from poolseq is vulnerable to experimental noise and bias at a number of protocol stages, from pooling equimolar ratios of DNA [ 66 ] through to library construction [ 67 ], sequencing and analysis.…”

Inferring Balancing Selection From Genome-Scale Data

“…Moreover, there is an increasing appreciation that BLS plays a role in fundamental biological processes such as sex determination ( Charlesworth 2004 ), self-incompatibility ( Lawrence 2000 ), and immune response ( Andrés et al 2009 ; Bitarello et al 2018 ). BLS can also shape the evolution of phenotypes directly related to survival, with recent studies illustrating that genome-wide heterozygosity may predict adult survival ( Doyle et al 2019 ; Scott et al 2020 ). By maintaining adaptive polymorphisms in populations, BLS is likely to maintain genetic diversity that contributes to evolutionarily relevant phenotypes, including those seen as diseases in extant populations ( Carter and Nguyen 2011 ).…”

Pitfalls and windfalls of detecting demographic declines using population genetics in long-lived species

“…Selection dynamics too will alter patterns seen in empirical systems. Inbreeding depression can result in viability selection, where adults in a population have higher heterozygosity because low-heterozygosity individuals do not reach adulthood due to deleterious homozygous genotypes (Clegg & Allard, 1973; Doyle et al, 2019; Labonne et al, 2016). Here we show that adults can have higher genetic diversity compared to juveniles due to purely neutral processes if there has been a recent population decline.…”