An official website of the United States government
ABSTRACT Identifying populations at highest risk from climate change is a critical component of conservation efforts. However, vulnerability assessments are usually applied at the species level, even though intraspecific variation in exposure, sensitivity and adaptive capacity play a crucial role in determining vulnerability. Genomic data can inform intraspecific vulnerability by identifying signatures of local adaptation that reflect population‐level variation in sensitivity and adaptive capacity. Here, we address the question of local adaptation to temperature and the genetic basis of thermal tolerance in two stream frogs (Ascaphus trueiandA. montanus). Building on previous physiological and temperature data, we used whole‐genome resequencing of tadpoles from four sites spanning temperature gradients in each species to test for signatures of local adaptation. To support these analyses, we developed the first annotated reference genome forA. truei. We then expanded the geographic scope of our analysis using targeted capture at an additional 11 sites per species. We found evidence of local adaptation to temperature based on physiological and genomic data inA. montanusand genomic data inA. truei, suggesting similar levels of sensitivity (i.e., susceptibility) among populations regardless of stream temperature. However, invariant thermal tolerances across temperatures inA. trueisuggest that populations occupying warmer streams may be most sensitive. We identified high levels of evolutionary potential in both species based on genomic and physiological data. While further integration of these data is needed to comprehensively evaluate spatial variation in vulnerability, this work illustrates the value of genomics in identifying spatial patterns of climate change vulnerability.
more »
« less
This content will become publicly available on December 1, 2025
Recently Delisted Songbird Harbors Extensive Genomic Evidence of Inbreeding, Potentially Complicating Future Recovery
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
- Award ID(s):
- 2131469
- PAR ID:
- 10564576
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Evolutionary Applications
- Volume:
- 17
- Issue:
- 12
- ISSN:
- 1752-4571
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Management strategies, such as assisted gene flow, can increase resilience to climate change in tree populations. Knowledge of evolutionary history and genetic structure of species are needed to assess the risks and benefits of different strategies.Quercus tomentella, or Island Oak, is a rare oak restricted to six Channel Islands in California, United States, and Baja California, Mexico. Previous work has shown that Island Oaks on each island are genetically differentiated, but it is unclear whether assisted gene flow could enable populations to tolerate future climates. We performed whole‐genome sequencing on Island Oak individuals andQ. chrysolepis, a closely related species that hybridizes with Island Oak (127 total), to characterize genetic structure and introgression across its range and assess the relationship between genomic variation and climate. We introduce and assess three potential management strategies with different trade‐offs between conserving historic genetic structure and enabling populations to survive changing climates: the status quo approach; ecosystem preservation approach, which conserves the trees and their associated biodiversity; and species preservation approach, which conserves the species. We compare the impact of these approaches on predicted maladaptation to climate using Gradient Forest. We also introduce a climate suitability index to identify optimal pairs of seed sources and planting sites for approaches involving assisted gene flow. We found one island (Santa Rosa) that could benefit from the ecosystem preservation approach and also serve as a species preservation site. Overall, we find that both the ecosystem and species preservation approaches will do better than the status quo approach. If preserving Island Oak ecosystems is the goal, assisted dispersal into multiple sites could produce adapted populations. If the goal is to preserve a species, the Santa Rosa population would be suitable. This case study both illustrates viable conservation strategies for Island Oak and introduces a framework for tree conservation.more » « less
-
ABSTRACT Yellow monkeyflowers (Mimulus guttatuscomplex, Phrymaceae) are a powerful system for studying ecological adaptation, reproductive variation, and genome evolution. To initiate pan‐genomics in this group, we present four chromosome‐scale assemblies and annotations of accessions spanning a broad evolutionary spectrum: two from a singleM. guttatuspopulation, one from the closely related selfing speciesM. nasutus, and one from a more divergent speciesM. tilingii. All assemblies are highly complete and resolve centromeric and repetitive regions. Comparative analyses reveal such extensive structural variation in repeat‐rich, gene‐poor regions that large portions of the genome are unalignable across accessions. As a result, thisMimuluspan‐genome is primarily informative in genic regions, underscoring limitations of resequencing approaches in such polymorphic taxa. We document gene presence–absence, investigate the recombination landscape using high‐resolution linkage data, and quantify nucleotide diversity. Surprisingly, pairwise differences at fourfold synonymous sites are exceptionally high—even in regions of very low recombination—reaching ~3.2% within a singleM. guttatuspopulation, ~7% within the interfertileM. guttatusspecies complex (approximately equal to SNP divergence between great apes and Old World monkeys), and ~7.4% between that complex and the reproductively isolatedM. tilingii. Genome‐wide patterns of nucleotide variation show little evidence of linked selection, and instead suggest that the concentration of genes (and likely selected sites) in high‐recombination regions may buffer diversity loss. These assemblies, annotations, and comparative analyses provide a robust genomic foundation forMimulusresearch and offer new insights into the interplay of recombination, structural variation, and molecular evolution in highly diverse plant genomes.more » « less
-
Abstract Next‐generation sequencing technologies now allow researchers of non‐model systems to perform genome‐based studies without the requirement of a (often unavailable) closely related genomic reference. We evaluated the role of restriction endonuclease (RE) selection in double‐digest restriction‐site‐associatedDNAsequencing (ddRADseq) by generating reduced representation genome‐wide data using four differentREcombinations. Our expectation was thatREselections targeting longer, more complex restriction sites would recover fewer loci thanREwith shorter, less complex sites. We sequenced a diverse sample of non‐model arachnids, including five congeneric pairs of harvestmen (Opiliones) and four pairs of spiders (Araneae). Sample pairs consisted of either conspecifics or closely related congeneric taxa, and in total 26 sample pair analyses were tested. Sequence demultiplexing, read clustering and variant calling were performed in thepyRADprogram. The 6‐base pair cutterEcoRIcombined with methylated site‐specific 4‐base pair cutterMspIproduced, on average, the greatest numbers of intra‐individual loci and shared loci per sample pair. As expected, the number of shared loci recovered for a sample pair covaried with the degree of genetic divergence, estimated with cytochrome oxidase I sequences, although this relationship was non‐linear. Our comparative results will prove useful in guiding protocol selection for ddRADseq experiments on many arachnid taxa where reference genomes, even from closely related species, are unavailable.more » « less
-
Abstract Copy number variation (CNV) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on atRNAligase gene (Migut.N02091;RLG1a) exhibiting unprecedented, and fitness‐relevant,CNVwithin an annual population of the yellow monkeyflowerMimulus guttatus.RLG1a variation was associated with multiple traits in pooled population sequencing (PoolSeq) scans of phenotypic and phenological cohorts. Resequencing of inbred lines revealed intermediate‐frequency three‐copy variants ofRLG1a (trip+;5/35 = 14%), andtrip+lines exhibited elevatedRLG1a expression under multiple conditions.trip+carriers, in addition to being over‐represented in late‐flowering and large‐flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (p < 0.05). In wild population samples, we discovered an additional rareRLG1a variant (high+) that carries 250–300 copies ofRLG1a totalling ~5.7 Mb (20–40% of a chromosome). In the progeny of ahigh+carrier, Mendelian segregation of diagnostic alleles andqPCR‐based copy counts indicate thathigh+is a single tandem array unlinked to the single‐copyRLG1a locus. In the wild,high+carriers had highest fitness in two particularly dry and/or hot years (2015 and 2017; bothp < 0.01), while single‐copy individuals were twice as fecund as eitherCNVtype in a lush year (2016:p < 0.005). Our results demonstrate fluctuating selection onCNVs affecting phenological traits in a wild population, suggest that planttRNAligases mediate stress‐responsive life‐history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification.more » « less
