An official website of the United States government
Although detrimental genetic processes are known to adversely affect the viability of populations, little is known about how detrimental genetic processes in a keystone species can affect the functioning of ecosystems. Here, we assessed how changes in the genetic characteristics of a keystone predator, grey wolves, affected the ecosystem of Isle Royale National Park over two decades. Changes in the genetic characteristic of the wolf population associated with a genetic rescue event, followed by high levels of inbreeding, led to a rise and then fall in predation rates on moose, the primary prey of wolves and dominant mammalian herbivore in this system. Those changes in predation rate led to large fluctuations in moose abundance, which in turn affected browse rates on balsam fir, the dominant forage for moose during winter and an important boreal forest species. Thus, forest dynamics can be traced back to changes in the genetic characteristics of a predator population.
more »
« less
Genomic Underpinnings of Population Persistence in Isle Royale Moose
Abstract Island ecosystems provide natural laboratories to assess the impacts of isolation on population persistence. However, most studies of persistence have focused on a single species, without comparisons to other organisms they interact with in the ecosystem. The case study of moose and gray wolves on Isle Royale allows for a direct contrast of genetic variation in isolated populations that have experienced dramatically differing population trajectories over the past decade. Whereas the Isle Royale wolf population recently declined nearly to extinction due to severe inbreeding depression, the moose population has thrived and continues to persist, despite having low genetic diversity and being isolated for ∼120 years. Here, we examine the patterns of genomic variation underlying the continued persistence of the Isle Royale moose population. We document high levels of inbreeding in the population, roughly as high as the wolf population at the time of its decline. However, inbreeding in the moose population manifests in the form of intermediate-length runs of homozygosity suggestive of historical inbreeding and purging, contrasting with the long runs of homozygosity observed in the smaller wolf population. Using simulations, we confirm that substantial purging has likely occurred in the moose population. However, we also document notable increases in genetic load, which could eventually threaten population viability over the long term. Overall, our results demonstrate a complex relationship between inbreeding, genetic diversity, and population viability that highlights the use of genomic datasets and computational simulation tools for understanding the factors enabling persistence in isolated populations.
more »
« less
- Award ID(s):
- 1939399
- PAR ID:
- 10479407
- Editor(s):
- Nielsen, Rasmus
- Publisher / Repository:
- Oxford Academic
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 40
- Issue:
- 2
- ISSN:
- 0737-4038
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Genetic rescue, specifically translocation to facilitate gene flow among populations and reduce the effects of inbreeding, is an increasingly used approach in conservation. However, this approach comes with trade‐offs, wherein gene flow may reduce fitness when populations have adaptive differentiation (i.e., outbreeding depression). A better understanding of the interaction between isolation, inbreeding, and adaptive divergence in key traits, such as life history traits, will help to inform genetic rescue efforts. Stream‐dwelling salmonids, such as the westslope cutthroat trout (Oncorhynchus lewisi; WCT), are well‐suited for examining these trade‐offs because they are increasingly isolated by habitat degradation, exhibit substantial variation in life history traits among populations, and include many species of conservation concern. However, few genomic studies have examined the potential trade‐offs in inbreeding versus outbreeding depression in salmonids. We used > 150,000 SNPs to examine genomic variation and inbreeding coefficients in 565 individuals across 25 WCT populations that differed in their isolation status and demographic histories. Analyses of runs of homozygosity revealed that several isolated WCT populations had “flatlined” having extremely low genetic variation and high inbreeding coefficients. Additionally, we conducted genome scans to identify potential outlier loci that could explain life history differences among 10 isolated populations. Genome scans identified one candidate genomic region that influenced maximum length and age‐1 to age‐2 growth. However, the limited number of candidate loci suggests that the life history traits examined may be driven by many genes of small effect or phenotypic plasticity. Although adaptive differentiation should be considered, the high inbreeding coefficients in several populations suggest that genetic rescue may benefit the most genetically depauperate WCT populations.more » « less
-
Abstract Theory predicts that threatened species living in small populations will experience high levels of inbreeding that will increase their genetic load, but recent work suggests that the impact of load may be minimized by purging resulting from long‐term population bottlenecks. Empirical studies that examine this idea using genome‐wide estimates of inbreeding and genetic load in threatened species are limited. Here we use individual genome resequencing data to compare levels of inbreeding, levels of genetic load (estimated as mutation load) and population history in threatened Eastern massasauga rattlesnakes (Sistrurus catenatus), which exist in small isolated populations, and closely related yet outbred Western massasauga rattlesnakes (Sistrurus tergeminus). In terms of inbreeding,S. catenatusgenomes had a greater number of runs of homozygosity of varying sizes, indicating sustained inbreeding through repeated bottlenecks when compared toS. tergeminus. At the species level, outbredS. tergeminushad higher genome‐wide levels of mutation load in the form of greater numbers of derived deleterious mutations compared toS. catenatus, presumably due to long‐term purging of deleterious mutations inS. catenatus. In contrast, mutations that escaped species‐level drift effects withinS. catenatuspopulations were in general more frequent and more often found in homozygous genotypes than inS. tergeminus, suggesting a reduced efficiency of purifying selection in smallerS. catenatuspopulations for most mutations. Our results support an emerging idea that the historical demography of a threatened species has a significant impact on the type of genetic load present, which impacts implementation of conservation actions such as genetic rescue.more » « less
-
Enard, David (Ed.)Abstract High-quality reference genomes are fundamental tools for understanding population history, and can provide estimates of genetic and demographic parameters relevant to the conservation of biodiversity. The federally endangered Pacific pocket mouse (PPM), which persists in three small, isolated populations in southern California, is a promising model for studying how demographic history shapes genetic diversity, and how diversity in turn may influence extinction risk. To facilitate these studies in PPM, we combined PacBio HiFi long reads with Omni-C and Hi-C data to generate a de novo genome assembly, and annotated the genome using RNAseq. The assembly comprised 28 chromosome-length scaffolds (N50 = 72.6 MB) and the complete mitochondrial genome, and included a long heterochromatic region on chromosome 18 not represented in the previously available short-read assembly. Heterozygosity was highly variable across the genome of the reference individual, with 18% of windows falling in runs of homozygosity (ROH) >1 MB, and nearly 9% in tracts spanning >5 MB. Yet outside of ROH, heterozygosity was relatively high (0.0027), and historical Ne estimates were large. These patterns of genetic variation suggest recent inbreeding in a formerly large population. Currently the most contiguous assembly for a heteromyid rodent, this reference genome provides insight into the past and recent demographic history of the population, and will be a critical tool for management and future studies of outbreeding depression, inbreeding depression, and genetic load.more » « less
-
Abstract Understanding the genetic and fitness consequences of anthropogenic bottlenecks is crucial for biodiversity conservation. However, studies of bottlenecked populations combining genomic approaches with fitness data are rare. Theory predicts that severe bottlenecks deplete genetic diversity, exacerbate inbreeding depression and decrease population viability. However, actual outcomes are complex and depend on how a species’ unique demography affects its genetic load. We used population genetic and veterinary pathology data, demographic modelling, whole-genome resequencing and forward genetic simulations to investigate the genomic and fitness consequences of a near-extinction event in the northern elephant seal. We found no evidence of inbreeding depression within the contemporary population for key fitness components, including body mass, blubber thickness and susceptibility to parasites and disease. However, we detected a genomic signature of a recent extreme bottleneck (effective population size = 6; 95% confidence interval = 5.0–7.5) that will have purged much of the genetic load, potentially leading to the lack of observed inbreeding depression in our study. Our results further suggest that deleterious genetic variation strongly impacted the post-bottleneck population dynamics of the northern elephant seal. Our study provides comprehensive empirical insights into the intricate dynamics underlying species-specific responses to anthropogenic bottlenecks.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/molbev/msad021
