Title: Reciprocal transplant gardens as gold standard to detect local adaptation in grassland species: New opportunities moving into the 21st century
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.
Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.
IMPORTANCE
In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.
Potts, Abigail S.; Hunter, Mark D.(
, Ecology and Evolution)
Abstract
Phenotypic variability results from interactions between genotype and environment and is a major driver of ecological and evolutionary interactions. Measuring the relative contributions of genetic variation, the environment, and their interaction to phenotypic variation remains a fundamental goal of evolutionary ecology.
In this study, we assess the question: How do genetic variation and local environmental conditions interact to influence phenotype within a single population? We explored this question using seed from a single population of common milkweed,Asclepias syriaca, in northern Michigan. We first measured resistance and resistance traits of 14 maternal lines in two common garden experiments (field and greenhouse) to detect genetic variation within the population. We carried out a reciprocal transplant experiment with three of these maternal lines to assess effects of local environment on phenotype. Finally, we compared the phenotypic traits measured in our experiments with the phenotypic traits of the naturally growing maternal genets to be able to compare relative effect of genetic and environmental variation on naturally occurring phenotypic variation. We measured defoliation levels, arthropod abundances, foliar cardenolide concentrations, foliar latex exudation, foliar carbon and nitrogen concentrations, and plant growth.
We found a striking lack of correlation in trait expression of the maternal lines between the common gardens, or between the common gardens and the naturally growing maternal genets, suggesting that environment plays a larger role in phenotypic trait variation of this population. We found evidence of significant genotype‐by‐environment interactions for all traits except foliar concentrations of nitrogen and cardenolide. Milkweed resistance to chewing herbivores was associated more strongly with the growing environment. We observed no variation in foliar cardenolide concentrations among maternal lines but did observe variation among maternal lines in foliar latex exudation.
Overall, our data reveal powerful genotype‐by‐environment interactions on the expression of most resistance traits in milkweed.
Goebl, April M.; Kane, Nolan C.; Doak, Daniel F.; Rieseberg, Loren H.; Ostevik, Kate L.(
, Molecular Ecology)
Abstract
Conspecific populations living in adjacent but contrasting microenvironments represent excellent systems for studying natural selection. These systems are valuable because gene flow is expected to force genetic homogeneity except at loci experiencing divergent selection. A history of reciprocal transplant and common garden studies in such systems, and a growing number of genomic studies, have contributed to understanding how selection operates in natural populations. While selection can vary across different fitness components and life stages, few studies have investigated how this ultimately affects allele frequencies and the maintenance of divergence between populations. Here, we study two sunflower ecotypes in distinct, adjacent habitats by combining demographic models with genome‐wide sequence data to estimate fitness and allele frequency change at multiple life stages. This framework allows us to estimate that only local ecotypes are likely to experience positive population growth (λ > 1) and that the maintenance of divergent adaptation appears to be mediated via habitat‐ and life stage‐specific selection. We identify genetic variation, significantly driven by loci in chromosomal inversions, associated with different life history strategies in neighbouring ecotypes that optimize different fitness components and may contribute to the maintenance of distinct ecotypes.
Hanley, Torrance C.; Bowen, Jennifer L.; Kearns, Patrick J.; Hughes, A. Randall(
, Journal of Ecology)
Abstract
Nutrient enrichment impacts ecosystems globally. Population history, especially past resource environments, of numerically dominant plant species may affect their responses to subsequent changes in nutrient availability. Eutrophication can also alter plant–microbe interactions via direct effects on associated microbial communities or indirect effects on dominant species’ biomass production/allocation as a result of modified plant–soil interactions.
We combined a greenhouse common garden and a field reciprocal transplant of a salt marsh foundation species (Spartina alterniflora) within a long‐term, whole‐ecosystem, nutrient‐enrichment study to determine whether enrichment affects plant production and microbial community structure differently depending on plant population history. For the greenhouse portion, we collected 20S. alternifloragenotypes—10 from an enriched creek that had received elevated nutrient inputs for 10 years and 10 from an unenriched reference creek—and reared them in a common garden for 1 year. For the field portion, we conducted a 2‐year, fully crossed reciprocal transplant experiment with two gardens each at the enriched and unenriched sites; we examined the effects of source site (i.e. population history), garden site and plant genotype.
After 2 years, plants in enriched gardens had higher above‐ground biomass and altered below‐ground allocation compared to plants in unenriched gardens. However, performance also depended on plant population history: plants from the enriched site had decreased above‐ground and rhizome production compared to plants from the unenriched site, most notably in unenriched gardens. In addition, almost all above‐ and below‐ground traits varied depending on plant genotypic identity.
Effects of nutrient enrichment on the associated microbial community were also pronounced. Following 1 year in common garden, microbial community structure varied by plant population history andS. alternifloragenotypic identity. However, at the end of the reciprocal transplant, microbial communities differed primarily between enriched and unenriched gardens.
Synthesis. Nutrient enrichment can impact plant foundation species and associated soil microbes in the short term. Most importantly, nutrient enrichment can also have long‐lasting effects on plant populations and associated microbial communities that potentially compromise their ability to respond to changing resource conditions in the future.
Capblancq, Thibaut; Lachmuth, Susanne; Fitzpatrick, Matthew C.; Keller, Stephen R.(
, New Phytologist)
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.
Johnson, Loretta C., Galliart, Matthew B., Alsdurf, Jacob D., Maricle, Brian R., Baer, Sara G., Bello, Nora M., Gibson, David J., and Smith, Adam B. Reciprocal transplant gardens as gold standard to detect local adaptation in grassland species: New opportunities moving into the 21st century. Journal of Ecology 110.5 Web. doi:10.1111/1365-2745.13695.
Johnson, Loretta C., Galliart, Matthew B., Alsdurf, Jacob D., Maricle, Brian R., Baer, Sara G., Bello, Nora M., Gibson, David J., & Smith, Adam B. Reciprocal transplant gardens as gold standard to detect local adaptation in grassland species: New opportunities moving into the 21st century. Journal of Ecology, 110 (5). https://doi.org/10.1111/1365-2745.13695
Johnson, Loretta C., Galliart, Matthew B., Alsdurf, Jacob D., Maricle, Brian R., Baer, Sara G., Bello, Nora M., Gibson, David J., and Smith, Adam B.
"Reciprocal transplant gardens as gold standard to detect local adaptation in grassland species: New opportunities moving into the 21st century". Journal of Ecology 110 (5). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/1365-2745.13695.https://par.nsf.gov/biblio/10388043.
@article{osti_10388043,
place = {Country unknown/Code not available},
title = {Reciprocal transplant gardens as gold standard to detect local adaptation in grassland species: New opportunities moving into the 21st century},
url = {https://par.nsf.gov/biblio/10388043},
DOI = {10.1111/1365-2745.13695},
abstractNote = {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.},
journal = {Journal of Ecology},
volume = {110},
number = {5},
publisher = {Wiley-Blackwell},
author = {Johnson, Loretta C. and Galliart, Matthew B. and Alsdurf, Jacob D. and Maricle, Brian R. and Baer, Sara G. and Bello, Nora M. and Gibson, David J. and Smith, Adam B.},
}
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