Abstract Local adaptation is a fundamental phenomenon in evolutionary biology, with relevance to formation of ecotypes, and ultimately new species, and application to restoration and species’ response to climate change. Reciprocal transplant gardens, a common garden in which ecotypes are planted among home and away habitats, are the gold standard to detect local adaptation in populations.This review focuses on reciprocal transplant gardens to detect local adaptation, especially in grassland species beginning with early seminal studies of grass ecotypes. Fast forward more than half a century, reciprocal gardens have moved into the genomic era, in which the genetic underpinnings of ecotypic variation can now be uncovered. Opportunities to combine genomic and reciprocal garden approaches offer great potential to shed light on genetic and environmental control of phenotypic variation. Our decadal study of adaptation in a dominant grass across the precipitation gradient of the US Great Plains combined genomic approaches and realistic community settings to shed light on controls over phenotype.Common gardens are not without limitations and challenges. A survey of recent studies indicated the modal study uses a tree species, three source sites and one growing site, focuses on one species growing in a monoculture, lasts 3 years, and does not use other experimental manipulations and rarely employs population genetic tools. Reciprocal transplant gardens are even more uncommon, accounting for only 39% of the studies in the literature survey with the rest occurring at a single common site. Reciprocal transplant gardens offer powerful windows into local adaptation when (a) placed across wide environmental gradients to encompass the species’ range; (b) conducted across timespans adequate for detecting responses; (c) employing selection studies among competing ecotypes in community settings and (d) combined with measurements of form and function which ultimately determine success in home and away environments.Synthesis. Reciprocal transplant gardens have been one of the foundations in evolutionary biology for the study of adaptation for the last century, and even longer in Europe. Moving forward, reciprocal gardens of foundational non‐model species, combined with genomic analyses and incorporation of biotic factors, have the potential to further revolutionize evolutionary biology. These field experiments will help to predict and model response to climate change and inform restoration practices.
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:
- 10538161
- Publisher / Repository:
- Wiley-Blackwell
- 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
-
-
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
-
Summary 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 conditions. 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 correction 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
-
Abstract Co-adaptation of cytoplasmic and nuclear genomes are critical to physiological function for many species. Despite this understanding, hybridization can disrupt co-adaptation leading to a mismatch between maternally-inherited cytoplasmic genomes and biparentally inherited nuclear genomes. Few studies have examined the consequences of cytonuclear interactions to physiological function across environments. Here, we quantify the degree of co-introgression between chloroplast and nuclear-chloroplast (N-cp) genes across repeated hybrid zones and its consequences to physiological function across environments. We use whole-genome resequencing and common garden experiments with clonally replicated genotypes sampled across the natural hybrid zone betweenPopulus trichocarpaandP. balsamifera. We use geographic clines to test for co-introgression of the chloroplast genome with N-cp and non-interacting nuclear genes. Co-introgression of chloroplast and N-cp genes was limited although contact zone-specific patterns suggest that local environments may influence co-introgression. Combining ancestry estimates with phenotypic data across common gardens revealed that mismatches between chloroplast and nuclear ancestry can influence physiological performance, but the strength and direction of these effects vary depending on the environment. Overall, this study highlights the importance of cytonuclear interactions to adaptation, and the role of environment in modifying the effect of those interactions.more » « less
An official website of the United States government
