Abstract Stomata play a critical role in regulating plant responses to climate. Where sister species differ in stomatal traits, interspecific gene flow can influence the evolutionary trajectory of trait variation, with consequences to adaptation.Leveraging six latitudinally-distributed transects spanning the natural hybrid zone betweenPopulus trichocarpa–P. balsamifera, we used whole genome resequencing and replicate common garden experiments to test the role that interspecific gene flow and selection play to stomatal trait evolution.While species-specific differences in the distribution of stomata persist betweenP. balsamiferaandP. trichocarpa, hybrids on average resembledP. trichocarpa. Admixture mapping identified several candidate genes associated with stomatal trait variation in hybrids includingTWIST, a homolog ofSPEECHLESSinArabidopsis, that initiates stomatal development via asymmetric cell divisions. Geographic clines revealed candidate genes deviating from genome-wide average patterns of introgression, suggesting restricted gene flow and the maintenance of adaptive differences. Climate associations, particularly with precipitation, indicated selection shapes local ancestry at candidate genes across transects.These results highlight the role of climate in shaping stomatal trait evolution inPopulusand demonstrate how interspecific gene flow creates novel genetic combinations that may enhance adaptive potential in changing environments.
more »
« less
Mutational load and adaptive variation are shaped by climate and species range dynamics in Vitis arizonica
Summary Genetic load can reduce fitness and hinder adaptation. While its genetic underpinnings are well established, the influence of environmental variation on genetic load is less well characterized, as is the relationship between genetic load and putatively adaptive genetic variation. This study examines the interplay among climate, species range dynamics, adaptive variation, and mutational load – a genomic measure of genetic load – inVitis arizonica, a wild grape native to the American Southwest.We estimated mutational load and identified climate‐associated adaptive genetic variants in 162 individuals across the species' range. Using a random forest model, we analyzed the relationship between mutational load, climate, and range shifts.Our findings linked mutational load to climatic variation, historical dispersion, and heterozygosity. Populations at the leading edge of range expansion harbored higher load and fewer putatively adaptive alleles associated with climate. Climate projections suggest thatV. arizonicawill expand its range by the end of the century, accompanied by a slight increase in mutational load at the population level.This study advances understanding of how environmental and geographic factors shape genetic load and adaptation, highlighting the need to integrate deleterious variation into broader models of species response to climate change.
more »
« less
- Award ID(s):
- 2414478
- PAR ID:
- 10647913
- Publisher / Repository:
- New Phytologist
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 247
- Issue:
- 2
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- 998 to 1014
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Global change is impacting biodiversity across all habitats on earth. New selection pressures from changing climatic conditions and other anthropogenic activities are creating heterogeneous ecological and evolutionary responses across many species' geographic ranges. Yet we currently lack standardised and reproducible tools to effectively predict the resulting patterns in species vulnerability to declines or range changes.We developed an informatic toolbox that integrates ecological, environmental and genomic data and analyses (environmental dissimilarity, species distribution models, landscape connectivity, neutral and adaptive genetic diversity, genotype‐environment associations and genomic offset) to estimate population vulnerability. In our toolbox, functions and data structures are coded in a standardised way so that it is applicable to any species or geographic region where appropriate data are available, for example individual or population sampling and genomic datasets (e.g. RAD‐seq, ddRAD‐seq, whole genome sequencing data) representing environmental variation across the species geographic range.To demonstrate multi‐species applicability, we apply our toolbox to three georeferenced genomic datasets for co‐occurring East African spiny reed frogs (Afrixalus fornasini, A. delicatusandA. sylvaticus) to predict their population vulnerability, as well as demonstrating that range loss projections based on adaptive variation can be accurately reproduced from a previous study using data for two European bat species (Myotis escaleraiandM. crypticus).Our framework sets the stage for large scale, multi‐species genomic datasets to be leveraged in a novel climate change vulnerability framework to quantify intraspecific differences in genetic diversity, local adaptation, range shifts and population vulnerability based on exposure, sensitivity and landscape barriers.more » « less
-
Abstract Identifying genomic adaptation is key to understanding species' evolutionary responses to environmental changes. However, current methods to identify adaptive variation have two major limitations. First, when estimating genetic variation, most methods do not account for observational uncertainty in genetic data because of finite sampling and missing genotypes. Second, many current methods use phenomenological models to partition genetic variation into adaptive and non‐adaptive components.We address these limitations by developing a hierarchical Bayesian model that explicitly accounts for observational uncertainty and underlying evolutionary processes. The first layer of the hierarchy is the data model that captures observational uncertainty by probabilistically linking RAD sequence data to genetic variation. The second layer is a process model that represents how evolutionary forces, such as local adaptation, mutation, migration and drift, maintain genetic variation. The third layer is the parameter model, which incorporates our knowledge about biological processes. For example, because most loci in the genome are expected to be neutral, the environmental sensitivity coefficients are assigned a regularized prior centred at zero. Together, the three models provide a rigorous probabilistic framework to identify local adaptation in wild organisms.Analysis of simulated RAD‐seq data shows that our statistical model can reliably infer adaptive genetic variation. To show the real‐world applicability of our method, we re‐analysed RAD‐Seq data (~105 k SNPs) from Willow Flycatchers (Empidonax traillii) in the United States. We found 30 genes close to 47 loci that showed a statistically significant association with temperature seasonality. Gene ontology suggests that several of these genes play a crucial role in egg mineralization, feather development and the ability to withstand extreme temperatures.Moreover, the data and process models can be modified to accommodate a wide range of genetic datasets (e.g. pool and low coverage genome sequencing) and demographic histories (e.g. range shifts) to study climatic adaptation in a wide range of natural systems.more » « less
-
Summary Joshua trees are long‐lived perennial monocots native to the Mojave Desert in North America. Composed of two species,Yucca brevifoliaandY. jaegeriana(Asparagaceae), Joshua trees are imperiled by climate change, with decreases in suitable habitat predicted under future climate change scenarios. Relatively little is understood about the ecophysiology of Joshua trees across their range, including the extent to which populations are locally adapted or phenotypically plastic to environmental stress.Plants in our common gardens showed evidence of Crassulacean acid metabolism photosynthesis (CAM) in a pilot experiment, despite no prior report of this photosynthetic pathway in these species. We further studied the variation and strength of CAM within a single common garden, measuring seedlings representing populations across the range of the two species.A combination of physiology and transcriptomic data showed low levels of CAM that varied across populations but were unrelated to home environmental conditions. Gene expression confirmed CAM activity and further suggested differences in carbon and nitrogen metabolism betweenY. brevifoliaandY. jaegeriana.Together the results suggest greater physiological diversity between these species than initially expected, particularly at the seedling stage, with implications for future survival of Joshua trees under a warming climate.more » « less
-
Summary Plastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype‐specific reaction norms across the continuum of historic and future climate conditions comprising a species' range.The North American hybrid zone ofPopulus trichocarpaandPopulus balsamiferarepresents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 44 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over 2 yr, enabling us to model reaction norms for each genotype across these tested environments.Species ancestry and intraspecific genomic variation significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade‐off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with moreP. trichocarpaancestry may gain an advantage under warmer climates.Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape‐level effects.more » « less
An official website of the United States government

