skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Balancing Inbreeding and Outbreeding Risks to Inform Translocations Throughout the Range of an Imperiled Darter
ABSTRACT Restoring connectivity via assisted migration is a useful but currently underused approach for maintaining genetic diversity and preventing extirpations of threatened species. The use of assisted migration as a conservation strategy may be limited by the difficulty of balancing the benefits of reconnecting populations (including reduced inbreeding depression and increased adaptive capacity) with the perceived risk of outbreeding depression, which requires comprehensive knowledge of the landscape of adaptive, neutral, deleterious, and structural variation across a species' range. Using a combination of reduced‐representation and whole‐genome sequencing, we characterized genomic diversity and differentiation for the Arkansas Darter (Etheostoma cragini) across its range in the Midwestern US. We found strong population structure and large differences in genetic diversity and effective population sizes across drainages. The strength of genetic isolation by river distance differed among drainages, with landscape type surrounding streams and impoundments also contributing to genetic isolation. Despite low effective population sizes in some populations, there was surprisingly little evidence for recent inbreeding (based on the absence of long runs of homozygosity) or for elevated levels of deleterious variation in smaller populations. Considering neutral, adaptive, deleterious, and structural variation allowed us to identify several potential recipient populations that may benefit from translocations and potential donor sites throughout the range. Planning translocation strategies intended for restored connectivity and possible genetic rescue at earlier stages in species decline will likely increase the probability of retaining genetic diversity and population persistence over the long term while minimizing risks associated with translocation.  more » « less
Award ID(s):
2016569
PAR ID:
10660591
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Evolutionary Applications
Date Published:
Journal Name:
Evolutionary Applications
Volume:
18
Issue:
3
ISSN:
1752-4571
Page Range / eLocation ID:
e70088
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest‐dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation‐by‐distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas. 
    more » « less
  2. 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
  3. Purugganan, Michael (Ed.)
    Abstract The deleterious effects of inbreeding have been of extreme importance to evolutionary biology, but it has been difficult to characterize the complex interactions between genetic constraints and selection that lead to fitness loss and recovery after inbreeding. Haploid organisms and selfing organisms like the nematode Caenorhabditis elegans are capable of rapid recovery from the fixation of novel deleterious mutation; however, the potential for recovery and genomic consequences of inbreeding in diploid, outcrossing organisms are not well understood. We sought to answer two questions: 1) Can a diploid, outcrossing population recover from inbreeding via standing genetic variation and new mutation? and 2) How does allelic diversity change during recovery? We inbred C. remanei, an outcrossing relative of C. elegans, through brother-sister mating for 30 generations followed by recovery at large population size. Inbreeding reduced fitness but, surprisingly, recovery from inbreeding at large populations sizes generated only very moderate fitness recovery after 300 generations. We found that 65% of ancestral single nucleotide polymorphisms (SNPs) were fixed in the inbred population, far fewer than the theoretical expectation of ∼99%. Under recovery, 36 SNPs across 30 genes involved in alimentary, muscular, nervous, and reproductive systems changed reproducibly across replicates, indicating that strong selection for fitness recovery does exist. Our results indicate that recovery from inbreeding depression via standing genetic variation and mutation is likely to be constrained by the large number of segregating deleterious variants present in natural populations, limiting the capacity for recovery of small populations. 
    more » « less
  4. The Kirtland's warbler (Setophaga kirtlandi) is a rare migratory passerine species and habitat specialist of the North American Jack Pine Forests. Their near extinction in the 1970s classified them as endangered and protected under the Endangered Species Act of 1973. After decades of intense conservation management, their population size recovered, and they were delisted from federal protection in 2019. We explore the genomic consequences of this harsh bottleneck and recovery by comparing the genomic architecture of two closely related species whose population sizes have remained large and stable, Hooded Warblers (Setophaga citrina) and American Redstarts (Setophaga ruticilla). We used whole‐genome sequencing to characterize the distribution of runs of homozygosity and deleterious genetic variation. We find evidence that Kirtland's warblers exhibit genetic patterns consistent with recent inbreeding. Our results also show that Kirtland's warblers carry an excess proportion of deleterious variation, which could complicate management for this conservation‐reliant species. This analysis provides a genetically informed perspective that should be thoroughly considered when delisting other species from federal protections. Through the increasing accessibility of genome sequencing technology, it will be more feasible to monitor the genetic landscape of recovering populations to ensure their long‐term survival independent of conservation intervention. 
    more » « less
  5. 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