Genomic Consequences of Population Decline in the Endangered Florida Scrub-Jay

Abstract

Summary Understanding the population genetic consequences of declining population size is important for conserving the many species worldwide facing severe decline [1]. Thorough empirical studies on the impacts of population reduction at a genome-wide scale in the wild are scarce because they demand huge field and laboratory investments [1, 2]. Previous studies have demonstrated the importance of gene flow in introducing genetic variation to small populations [3], but few have documented both genetic and fitness consequences of decreased immigration through time in a natural population [4-6]. Here we assess temporal variation in gene flow, inbreeding, and fitness using longitudinal genomic, demographic, and phenotypic data from a long-studied population of federally Threatened Florida Scrub-Jays (Aphelocoma coerulescens; hereafter FSJ). We exhaustively sampled and genotyped the study population over two decades, providing one of the most detailed longitudinal investigations of genetics in a wild animal population to date. Immigrants were less heterozygous than residents but still introduced genetic variation into our study population. Owing to regional population declines, immigration into the study population declined from 1995-2013, resulting in increased levels of inbreeding and reduced fitness via inbreeding depression, even as the population remained demographically stable. Our results show that, contrary to conventional wisdom, small peripheral populations that already have undergone a genetic bottleneck may play a vital role in preserving genetic diversity of larger and seemingly stable populations. These findings underscore the importance of investing in the persistence of small populations and maintaining population connectivity in conservation of fragmented species.

Allele frequency dynamics in a pedigreed natural population

“…The high expected genetic contribution of immigrants is consistent with previous results showing that immigrants play an important role in maintaining levels of genetic variation in the population (19). Genomewide, allele frequency changes are primarily driven by variation in individual survival and reproduction.…”

“…Previous work showed high levels of immigration into our study population (19), with immigrants comprising 32-55% of all breeding adults in a given year (19). We estimated the cumulative expected genetic contribution of new immigrants appearing in our study population from 1991 onward ( Fig.…”

“…Because of the very low rate of extra-pair paternity and limited natal dispersal distances in this population (19)(20)(21)33), we have a detailed and accurate population pedigree. To avoid any artifacts caused by study tract expansion before 1990, we began all our analyses in 1990 and truncated the pedigree accordingly.…”

“…In a previous study, we genotyped 3,984 individuals at 15,416 genome-wide SNPs, resulting in near-complete sampling of all nestlings and breeders in these core territories in 1989-1991, 1995, and 1999-2013 (19). Information on SNP discovery, genotyping, and pedigree verification can be found in (19). Here, we removed SNPs with minor allele frequency < 0.05.…”

“…Intensive study since 1969 has resulted in lifetime fitness measures for thousands of individuals on an extensive pedigree. Recently, Chen et al (19) generated genome-wide single nucleotide polymorphism (SNP) data for nearly every individual in the population over the past two decades. In this study, we link individual lifetime reproductive success with long-term genetic contributions and allele frequency change.…”