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
The accuracy of predicting maladaptation to new environments with genomic data
Abstract Rapid environmental change poses unprecedented challenges to species persistence. To understand the extent that continued change could have, genomic offset methods have been used to forecast maladaptation of natural populations to future environmental change. However, while their use has become increasingly common, little is known regarding their predictive performance across a wide array of realistic and challenging scenarios. Here, we evaluate the performance of currently available offset methods (gradientForest, the Risk‐Of‐Non‐Adaptedness, redundancy analysis with and without structure correction and LFMM2) using an extensive set of simulated data sets that vary demography, adaptive architecture and the number and spatial patterns of adaptive environments. For each data set, we train models using eitherall,adaptiveorneutralmarker sets and evaluate performance using in silico common gardens by correlating known fitness with projected offset. Using over 4,849,600 of such evaluations, we find that (1) method performance is largely due to the degree of local adaptation across the metapopulation (LA), (2)adaptivemarker sets provide minimal performance advantages, (3) performance within the species range is variable across gardens and declines when offset models are trained using additional non‐adaptive environments and (4) despite (1) performance declines more rapidly in globally novel climates (i.e. a climate without an analogue within the species range) for metapopulations with greaterLAthan lesserLA. We discuss the implications of these results for management, assisted gene flow and assisted migration.
more »
« less
- Award ID(s):
- 2043905
- PAR ID:
- 10582471
- Publisher / Repository:
- Molecular Ecology Resources
- Date Published:
- Journal Name:
- Molecular Ecology Resources
- Volume:
- 25
- Issue:
- 4
- ISSN:
- 1755-098X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
-Local adaptation to climate is common in plant species and has been studied in a range of contexts, from improving crop yields to predicting population maladaptation to future condi- tions. The genomic era has brought new tools to study this process, which was historically explored through common garden experiments. - In this study, we combine genomic methods and common gardens to investigate local adaptation in red spruce and identify environmental gradients and loci involved in climate adaptation. We first use climate transfer functions to estimate the impact of climate change on seedling performance in three common gardens. We then explore the use of multivariate gene–environment association methods to identify genes underlying climate adaptation, with particular attention to the implications of conducting genome scans with and without correc- tion for neutral population structure. -This integrative approach uncovered phenotypic evidence of local adaptation to climate and identified a set of putatively adaptive genes, some of which are involved in three main adaptive pathways found in other temperate and boreal coniferous species: drought tolerance, cold hardiness, and phenology. These putatively adaptive genes segregated into two ‘modules’ associated with different environmental gradients. -This study nicely exemplifies the multivariate dimension of adaptation to climate in trees.more » « less
-
Selection on quantitative traits by heterogeneous climatic conditions can lead to substantial trait variation across a species range. In the context of rapidly changing environments, however, it is equally important to understand selection on trait plasticity. To evaluate the role of selection in driving divergences in traits and their associated plasticities within a widespread species, we compared molecular and quantitative trait variation in Populus fremontii (Fremont cottonwood), a foundation riparian distributed throughout Arizona. Using SNP data and genotypes from 16 populations reciprocally planted in three common gardens, we first performed QST-FST analyses to detect selection on traits and trait plasticity. We then explored the environmental drivers of selection using trait-climate and plasticity-climate regressions. Three major findings emerged: 1) There was significant genetic variation in traits expressed in each of the common gardens and in the phenotypic plasticity of traits across gardens, both of which were heritable. 2) Based on QST-FST comparisons, there was evidence of selection in all traits measured; however, this result varied from no effect in one garden to highly significant in another, indicating that detection of past selection is environmentally dependent. We also found strong evidence of divergent selection on plasticity across environments for two traits. 3) Traits and/or their plasticity were often correlated with population source climate (R2 up to 0.77 and 0.66, respectively). These results suggest that steep climate gradients across the Southwest have played a major role in shaping the evolution of divergent phenotypic responses in populations and genotypes now experiencing climate change.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
-
Shifting range limits are predicted for many species as the climate warms. However, the rapid pace of climate change will challenge the natural dispersal capacity of long-lived, sessile organisms such as forest trees. Adaptive responses of populations will, therefore, depend on levels of genetic variation and plasticity for climate-responsive traits, which likely vary across the range due to expansion history and current patterns of selection. Here, we study levels of genetic and plastic variation for phenology and growth traits in populations of red spruce ( Picea rubens ), from the range core to the highly fragmented trailing edge. We measured more than 5000 offspring sampled from three genetically distinct regions (core, margin and edge) grown in three common gardens replicated along a latitudinal gradient. Genetic variation in phenology and growth showed low to moderate heritability and differentiation among regions, suggesting some potential to respond to selection. Phenology traits were highly plastic, but this plasticity was generally neutral or maladaptive in the effect on growth, revealing a potential liability under warmer climates. These results suggest future climate adaptation will depend on the regional availability of genetic variation in red spruce and provide a resource for the design and management of assisted gene flow. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’.more » « less
An official website of the United States government

