skip to main content


Title: Genomic signatures of inbreeding and mutation load in a threatened rattlesnake
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,Scatenatusgenomes had a greater number of runs of homozygosity of varying sizes, indicating sustained inbreeding through repeated bottlenecks when compared toStergeminus. At the species level, outbredStergeminushad higher genome‐wide levels of mutation load in the form of greater numbers of derived deleterious mutations compared toScatenatus, presumably due to long‐term purging of deleterious mutations inScatenatus. In contrast, mutations that escaped species‐level drift effects withinScatenatuspopulations were in general more frequent and more often found in homozygous genotypes than inStergeminus, suggesting a reduced efficiency of purifying selection in smallerScatenatuspopulations 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
Award ID(s):
1638872
NSF-PAR ID:
10360202
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
30
Issue:
21
ISSN:
0962-1083
Page Range / eLocation ID:
p. 5454-5469
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    An important goal of conservation genetics is to determine if the viability of small populations is reduced by a loss of adaptive variation due to genetic drift. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the eastern massasauga rattlesnake (Sistrurus catenatus), a threatened reptile that exists in small isolated populations. We estimated levels of individual polymorphism in 46 toxin loci and 1,467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation ofS. catenatusand its closest relative, the western massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long‐ and short‐term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that pre‐date the effects of recent drift, and that functional variation in these loci persists despite small short‐term effective sizes. This suggests that much of the adaptive variation present in populations may represent an example of “drift debt,” a nonequilibrium state where present‐day levels of variation overestimate the amount of functional genetic diversity present in future populations.

     
    more » « less
  2. Abstract

    Managing endangered species in fragmented landscapes requires estimating dispersal rates between populations over contemporary timescales. Here, we developed a new method for quantifying recent dispersal using genetic pedigree data for close and distant kin. Specifically, we describe an approach that infers missing shared ancestors between pairs of kin in habitat patches across a fragmented landscape. We then applied a stepping‐stone model to assign unsampled individuals in the pedigree to probable locations based on minimizing the number of movements required to produce the observed locations in sampled kin pairs. Finally, we used all pairs of reconstructed parent‐offspring sets to estimate dispersal rates between habitat patches under a Bayesian model. Our approach measures connectivity over the timescale represented by the small number of generations contained within the pedigree and so is appropriate for estimating the impacts of recent habitat changes due to human activity. We used our method to estimate recent movement between newly discovered populations of threatened Eastern Massasauga rattlesnakes (Sistrurus catenatus) using data from 2996 RAD‐based genetic loci. Our pedigree analyses found no evidence for contemporary connectivity between five genetic groups, but, as validation of our approach, showed high dispersal rates between sample sites within a single genetic cluster. We conclude that these five genetic clusters of Eastern Massasauga rattlesnakes have small numbers of resident snakes and are demographically isolated conservation units. More broadly, our methodology can be widely applied to determine contemporary connectivity rates, independent of bias from shared genetic similarity due to ancestry that impacts other approaches.

     
    more » « less
  3. Small populations with limited range are often threatened by inbreeding and reduced genetic diversity, which can reduce fitness and exacerbate population decline. One of the most extreme natural examples is the Devils Hole pupfish ( Cyprinodon diabolis ), an iconic and critically endangered species with the smallest known range of any vertebrate. This species has experienced severe declines in population size over the last 30 years and suffered major bottlenecks in 2007 and 2013, when the population shrunk to 38 and 35 individuals, respectively. Here, we analysed 30 resequenced genomes of desert pupfishes from Death Valley, Ash Meadows and surrounding areas to examine the genomic consequences of small population size. We found extremely high levels of inbreeding ( F ROH = 0.34–0.81) and an increased amount of potentially deleterious genetic variation in the Devils Hole pupfish as compared to other species, including unique, fixed loss-of-function alleles and deletions in genes associated with sperm motility and hypoxia. Additionally, we successfully resequenced a formalin-fixed museum specimen from 1980 and found that the population was already highly inbred prior to recent known bottlenecks. We thus document severe inbreeding and increased mutation load in the Devils Hole pupfish and identify candidate deleterious variants to inform management of this conservation icon. 
    more » « less
  4. Abstract

    Assessing the environmental factors that influence the ability of a threatened species to move through a landscape can be used to identify conservation actions that connect isolated populations. However, direct observations of species' movement are often limited, making the development of alternate approaches necessary. Here we use landscape genetic analyses to assess the impact of landscape features on the movement of individuals between local populations of a threatened snake, the eastern massasauga rattlesnake (Sistrurus catenatus). We linked connectivity data with habitat information from two landscapes of similar size: a large region of unfragmented habitat and a previously studied fragmented landscape consisting of isolated patches of habitat. We used this analysis to identify features of the landscape where modification or acquisition would enhance population connectivity in the fragmented region. We found evidence that current connectivity was impacted by both contemporary land‐cover features, especially roads, and inherent landscape features such as elevation. Next, we derived estimates of expected movement ability using a recently developed pedigree‐based approach and least‐cost paths through the unfragmented landscape. We then used our pedigree and resistance map to estimate resistance polygons of the potential extent forS. catenatusmovement in the fragmented landscape. These polygons identify possible sites for future corridors connecting currently isolated populations in this landscape by linking the impact of future habitat modification or land acquisition to dispersal ability in this species. Overall, our study shows how modeling landscape resistance across differently fragmented landscapes can identify habitat features that affect contemporary movement in threatened species in fragmented landscapes and how this information can be used to guide mitigation actions whose goal is to connect isolated populations.

     
    more » « less
  5. Abstract

    Inbreeding exposes deleterious recessive alleles in homozygotes, lowering fitness and generating inbreeding depression (ID). Both purging (via selection) and fixation (via drift) should reduce segregating deleterious mutations and ID in more inbred populations. These theoretical predictions are not well-tested in wild populations, which is concerning given purging/fixation have opposite fitness outcomes. We examined how individual- and population-level inbreeding and genomic heterozygosity affected maternal and progeny fitness within and among 12 wild populations of Impatiens capensis. We quantified maternal fitness in home sites, maternal multilocus heterozygosity (using 12,560 single-nucleotide polymorphisms), and lifetime fitness of selfed and predominantly outcrossed progeny in a common garden. These populations spanned a broad range of individual-level (fi = −0.17–0.98) and population-level inbreeding (FIS = 0.25–0.87). More inbred populations contained fewer polymorphic loci, less fecund mothers, and smaller progeny, suggesting higher fixed loads. However, despite appreciable ID (mean: 8.8 lethal equivalents per gamete), ID did not systematically decline in more inbred population. More heterozygous mothers were more fecund and produced fitter progeny in outcrossed populations, but this pattern unexpectedly reversed in highly inbred populations. These observations suggest that persistent overdominance or some other force acts to forestall purging and fixation in these populations.

     
    more » « less