Environmental contributions to the evolution of trait differences in Geum triflorum: Implications for restoration.
Rosaceae
adaptation
alvar
common garden experiment
ecotype
evolvability
heritability
prairie
stomata
water-use efficiency
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
21
06
2022
received:
14
02
2022
accepted:
21
06
2022
pubmed:
25
9
2022
medline:
30
11
2022
entrez:
24
9
2022
Statut:
ppublish
Résumé
How the environment influences the distribution of trait variation across a species' range has important implications for seed transfer during restoration. Evolution across environments could influence fitness when individuals are transferred into new environments. Here, we evaluate the role the environment has had on the distribution of genetic variance for traits important to adaptation. In a common garden experiment, we quantified trait differentiation for populations of Geum triflorum sourced from three distinct ecoregions and evaluated the ability of climate to predict trait variation. Populations were sourced from the Manitoba and Great Lake alvar ecoregions that experience predictable extremes in seasonal water availability and the prairie ecoregion which exhibits unpredictable changes in water availability. Plants sourced from alvar ecoregions exhibited smaller but more stomata and greater intrinsic water-use efficiency relative to prairie plant populations, supporting the evolution of ecotypic differences. Estimates of standing genetic variance and heritable genetic variation for quantitative traits suggest alvar populations have greater adaptive potential. However, low evolvability suggests all populations likely have limited capacity to evolve in response to environmental change. These results highlight the importance of the environment in influencing the evolution and distribution of genetic differences across populations used as seed sources for restoration. Additionally, these data may inform recommendations for seed transfer across novel environments and our expectations of populations' adaptive potential.
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1822-1837Informations de copyright
© 2022 Botanical Society of America.
Références
Ahrens, C. W., M. E. Andrew, R. A. Mazanec, K. X. Ruthrof, A. Challis, G. Hardy, M. Byrne, et al. 2020. Plant functional traits differ in adaptability and are predicted to be differentially affected by climate change. Ecology and Evolution 10: 232-248.
Anderson, J. T., and Z. J. Gezon. 2015. Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae). Global Change Biology 21: 1689-1703.
Anderson, J. T., J. H. Willis, and T. Mitchell-Olds. 2011. Evolutionary genetics of plant adaptation. Trends in Genetics 27: 258-266.
Anderson, R. H., S. D. Fuhlendorf, and D. M. Engle. 2006. Soil nitrogen availability in tallgrass prairie under the fire-grazing interaction. Rangeland Ecology & Management 59: 625-631.
Arntz, M. A., and L. F. Delph. 2001. Pattern and process: evidence for the evolution of photosynthetic traits in natural populations. Oecologia 127: 455-467.
Aspinwall, M. J., D. B. Lowry, S. H. Taylor, T. E. Juenger, C. V Hawkes, M. V Johnson, J. R. Kiniry, and P. A. Fay. 2013. Genotypic variation in traits linked to climate and aboveground productivity in a widespread C4 grass: evidence for a functional trait syndrome. New Phytologist 199: 966-980.
Bairos-Novak, K. R., M. O. Hoogenboom, M. J. H. van Oppen, and S. R. Connolly. 2021. Coral adaptation to climate change: Meta-analysis reveals high heritability across multiple traits. Global Change Biology 27: 5694-5710.
Baythavong, B. S. 2011. Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: Selection favors adaptive plasticity in fine-grained environments. American Naturalist 178: 75-87.
Becklin, K. M., J. T. Anderson, L. M. Gerhart, S. M. Wadgymar, C. A. Wessinger, and J. K. Ward. 2016. Examining plant physiological responses to climate change through an evolutionary lens. Plant Physiology 172: 635-649.
Bengtsson, J., J. M. Bullock, B. Egoh, C. Everson, T. Everson, T. O'Connor, P. J. O'Farrell, et al. 2019. Grasslands-more important for ecosystem services than you might think. Ecosphere 10: e02582.
Bertel, C., P. Schönswetter, B. Frajman, A. Holzinger, and G. Neuner. 2017. Leaf anatomy of two reciprocally non-monophyletic mountain plants (Heliosperma spp.): Does heritable adaptation to divergent growing sites accompany the onset of speciation? Protoplasma 254: 1411-1420.
Braasch, J. E., L. N. Di Santo, Z. J. Tarble, J. R. Prasifka, and J. A. Hamilton. 2021. Testing for evolutionary change in restoration: a genomic comparison between ex situ, native, and commercial seed sources of Helianthus maximiliani. Evolutionary Applications 14: 2206-2220.
Broadhurst, L. M., A. Lowe, D. J. Coates, S. A. Cunningham, M. McDonald, P. A. Vesk, and C. Yates. 2008. Seed supply for broadscale restoration: maximizing evolutionary potential. Evolutionary Applications 1: 587-597.
Bucharova, A., O. Bossdorf, N. Hölzel, J. Kollmann, R. Prasse, and W. Durka. 2019. Mix and match: regional admixture provenancing strikes a balance among different seed-sourcing strategies for ecological restoration. Conservation Genetics 20: 7-17.
Bucharova, A., W. Durka, N. Hölzel, J. Kollmann, S. Michalski, and O. Bossdorf. 2017. Are local plants the best for ecosystem restoration? It depends on how you analyze the data. Ecology and Evolution 7: 10683-10689.
Catling, P. M., and V. R. Brownell. 1995. A review of the alvars of the Great Lakes region: distribution, floristic composition, biogeography and protection. Canadian Field-Naturalist 109: 143-171.
Cava, J. A., N. G. Perlut, and S. E. Travis. 2019. Heritability and evolvability of morphological traits of Savannah sparrows (Passerculus sandwichensis) breeding in agricultural grasslands. PLoS One 14: e0210472.
Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8: e1000357.
Comer, P. J., J. C. Hak, K. Kindscher, E. Muldavin, and J. Singhurst. 2018. Continent-scale landscape conservation design for temperate grasslands of the Great Plains and Chihuahuan Desert. Natural Areas Journal 38: 196-211.
Cotto, O., J. Wessely, D. Georges, G. Klonner, M. Schmid, S. Dullinger, W. Thuiller, and F. Guillaume. 2017. A dynamic eco-evolutionary model predicts slow response of alpine plants to climate warming. Nature Communications 8: 1-9.
Crow, T. M., S. E. Albeke, C. A. Buerkle, and K. M. Hufford. 2018. Provisional methods to guide species-specific seed transfer in ecological restoration. Ecosphere 9: e02059.
Crowe, K. A., and W. H. Parker. 2008. Using portfolio theory to guide reforestation and restoration under climate change scenarios. Climatic Change 89: 355-370.
Didiano, T. J., M. T. J. Johnson, and T. P. Duval. 2016. Disentangling the effects of precipitation amount and frequency on the performance of 14 grassland species. PLoS One 11: e0162310.
Dittberner, H., A. Korte, T. Mettler-Altmann, A. P. M. Weber, G. Monroe, and J. de Meaux. 2018. Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana. Molecular Ecology 27: 4052-4065.
Donohue, K. 2009. Completing the cycle: maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society, B, Biological Sciences 364: 1059-1074.
Drake, P. L., R. H. Froend, and P. J. Franks. 2013. Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. Journal of Experimental Botany 64: 495-505.
Dudley, S. A. 1996. Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50: 92-102.
Espeland, E. K., N. C. Emery, K. L. Mercer, S. A. Woolbright, K. M. Kettenring, P. Gepts, and J. R. Etterson. 2017. Evolution of plant materials for ecological restoration: insights from the applied and basic literature. Journal of Applied Ecology 54: 102-115.
Etterson, J. R., and R. G. Shaw. 2001. Constraint to adaptive evolution in response to global warming. Science 294: 151-154.
Falconer, D. S. 1996. Introduction to quantitative genetics. Pearson Education, Harlow, UK.
Farquhar, G. D., K. T. Hubick, A. G. Condon, and R. A. Richards. 1989. Carbon isotope fractionation and plant water-use efficiency. In P. W. Rundel, J. R. Ehleringer, and K. A. Nagy [eds.], Stable isotopes in ecological research. Ecological Studies, 68, 21-40. Springer, NY, NY, USA.
Farquhar, G. D., M. H. O'Leary, and J. A. Berry. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Functional Plant Biology 9: 121-137.
Galliart, M., N. Bello, M. Knapp, J. Poland, P. St Amand, S. Baer, B. Maricle, et al. 2019. Local adaptation, genetic divergence, and experimental selection in a foundation grass across the US Great Plains’ climate gradient. Global Change Biology 25: 850-868.
Gascoigne, W. R., D. Hoag, L. Koontz, B. A. Tangen, T. L. Shaffer, and R. A. Gleason. 2011. Valuing ecosystem and economic services across land-use scenarios in the Prairie Pothole Region of the Dakotas, USA. Ecological Economics 70: 1715-1725.
Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21: 394-407.
Gilbert, A. L., and D. B. Miles. 2019. Antagonistic responses of exposure to sublethal temperatures: adaptive phenotypic plasticity coincides with a reduction in organismal performance. American Naturalist 194: 344-355.
Guo, C., L. Ma, S. Yuan, and R. Wang. 2017. Morphological, physiological and anatomical traits of plant functional types in temperate grasslands along a large-scale aridity gradient in northeastern China. Scientific Reports 7: 1-10.
Hamilton, J., S. Flint, J. Lindstrom, K. Volk, R. Shaw, and M. Ahlering. 2020. Evolutionary approaches to seed sourcing for grassland restorations. New Phytologist 225: 2246-2248.
Hamilton, J. A., and C. G. Eckert. 2007. Population genetic consequences of geographic disjunction: a prairie plant isolated on Great Lakes alvars. Molecular Ecology 16: 1649-1660.
Hansen, T. F., and D. Houle. 2008. Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology 21: 1201-1219.
Hansen, T. F., C. Pélabon, and D. Houle. 2011. Heritability is not evolvability. Evolutionary Biology 38: 258-277.
Havens, K., P. Vitt, S. Still, A. T. Kramer, J. B. Fant, and K. Schatz. 2015. Seed sourcing for restoration in an era of climate change. Natural Areas Journal 35: 122-133.
Hoekstra, J. M., T. M. Boucher, T. H. Ricketts, and C. Roberts. 2005. Confronting a biome crisis: global disparities of habitat loss and protection. Ecology Letters 8: 23-29.
Hoffman, D. W., and C. Rasmussen. 2022. Absolute carbon stable isotope ratio in the Vienna Peedee Belemnite isotope reference determined by 1H NMR spectroscopy. Analytical Chemistry 94: 5240-5247.
Jump, A. S., and J. Penuelas. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8: 1010-1020.
Kawecki, T. J., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241.
Kulbaba, M. W., S. N. Sheth, R. E. Pain, V. M. Eckhart, and R. G. Shaw. 2019. Additive genetic variance for lifetime fitness and the capacity for adaptation in an annual plant. Evolution 73: 1746-1758.
Kulbaba, M. W., Z. Yoko, and J. A. Hamilton. 2021. Chasing the fitness optimum: temporal variation in the genetic and environmental expression of life-history traits for a perennial plant. bioRxiv https://www.biorxiv.org/content/10.1101/2021.10.12.464067v1. [Preprint].
Lande, R. 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution 46: 381-389.
Levins, R. 1963. Theory of fitness in a heterogeneous environment. II. Developmental flexibility and niche selection. American Naturalist 97: 75-90.
Lowry, D. B., K. D. Behrman, P. Grabowski, G. P. Morris, J. R. Kiniry, and T. E. Juenger. 2014. Adaptations between ecotypes and along environmental gradients in Panicum virgatum. American Naturalist 183: 682-692.
March-Salas, M., M. van Kleunen, and P. S. Fitze. 2019. Rapid and positive responses of plants to lower precipitation predictability. Proceedings of the Royal Society, B, Biological Sciences 286: 20191486.
Maricle, B. R., K. L. Caudle, K. J. Lindsey, S. G. Baer, and L. C. Johnson. 2017. Effects of extreme drought on photosynthesis and water potential of Andropogon gerardii (big bluestem) ecotypes in common gardens across Kansas. Transactions of the Kansas Academy of Science 120: 1-16.
McKay, J. K., C. E. Christian, S. Harrison, and K. J. Rice. 2005. “How local is local?”-a review of practical and conceptual issues in the genetics of restoration. Restoration Ecology 13: 432-440.
McMillan, C. 1959. The role of ecotypic variation in the distribution of the central grassland of North America. Ecological Monographs 29: 286-308.
Nguyen, H. T., and D. A. Sleper. 1983. Theory and application of half-sib matings in forage grass breeding. Theoretical and Applied Genetics 64: 187-196.
Olsen, J. T., K. L. Caudle, L. C. Johnson, S. G. Baer, and B. R. Maricle. 2013. Environmental and genetic variation in leaf anatomy among populations of Andropogon gerardii (Poaceae) along a precipitation gradient. American Journal of Botany 100: 1957-1968.
Pearce, D. W., S. Millard, D. F. Bray, and S. B. Rood. 2006. Stomatal characteristics of riparian poplar species in a semi-arid environment. Tree Physiology 26: 211-218.
Picotte, J. J., D. M. Rosenthal, J. M. Rhode, and M. B. Cruzan. 2007. Plastic responses to temporal variation in moisture availability: consequences for water use efficiency and plant performance. Oecologia 153: 821-832.
Pronger, J., D. I. Campbell, M. J. Clearwater, P. L. Mudge, S. Rutledge, A. M. Wall, and L. A. Schipper. 2019. Toward optimisation of water use efficiency in dryland pastures using carbon isotope discrimination as a tool to select plant species mixtures. Science of The Total Environment 665: 698-708.
Ramírez-Valiente, J. A., N. J. Deacon, J. Etterson, A. Center, J. P. Sparks, K. L. Sparks, T. Longwell, et al. 2018. Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides. Molecular Ecology 27: 2176-2192.
Reed, T. E., R. S. Waples, D. E. Schindler, J. J. Hard, and M. T. Kinnison. 2010. Phenotypic plasticity and population viability: the importance of environmental predictability. Proceedings of the Royal Society, B, Biological Sciences 277: 3391-3400.
Ruhsam, M., P. M. Hollingsworth, and R. A. Ennos. 2011. Early evolution in a hybrid swarm between outcrossing and selfing lineages in Geum. Heredity 107: 246-255.
Ruhsam, M., P. M. Hollingsworth, and R. A. Ennos. 2013. Patterns of mating, generation of diversity, and fitness of offspring in a Geum hybrid swarm. Evolution 67: 2728-2740.
Singmann, H., B. Bolker, J. Westfall, F. Aust, M. S. Ben-Shachar, S. Hojsgaard, J. Fox, et al. 2021. Package ‘afex’. Website: https://cran.r-project.org/web/packages/afex/index.html
Sun, J., C. Liu, J. Hou, and N. He. 2021. Spatial variation of stomatal morphological traits in grassland plants of the Loess Plateau. Ecological Indicators 128: 107857.
Vandepitte, K., O. Honnay, H. Jacquemyn, and I. Roldan-Ruiz. 2010. Effects of outcrossing in fragmented populations of the primarily selfing forest herb Geum urbanum. Evolutionary Ecology 24: 1353-1364.
VanWallendael, A., D. B. Lowry, and J. A. Hamilton. 2022. One hundred years into the study of ecotypes, new advances are being made through large-scale field experiments in perennial plant systems. Current Opinion in Plant Biology 66: 102152.
Wadgymar, S. M., S. C. Daws, and J. T. Anderson. 2017. Integrating viability and fecundity selection to illuminate the adaptive nature of genetic clines. Evolution Letters 1: 26-39.
Wang, T., A. Hamann, D. Spittlehouse, and C. Carroll. 2016. Locally downscaled and spatially customizable climate data for historical and future periods for North America. PLoS One 11: e0156720.
Wang, T., G. A. O'Neill, and S. N. Aitken. 2010. Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecological Applications 20: 153-163.
Wimberly, M. C., D. M. Narem, P. J. Bauman, B. T. Carlson, and M. A. Ahlering. 2018. Grassland connectivity in fragmented agricultural landscapes of the north-central United States. Biological Conservation 217: 121-130.
Yang, X., Y. Yang, C. Ji, T. Feng, Y. Shi, L. Lin, J. Ma, and J.-S. He. 2014. Large-scale patterns of stomatal traits in Tibetan and Mongolian grassland species. Basic and Applied Ecology 15: 122-132.
Yoko, Z. G., K. L. Volk, N. A. Dochtermann, and J. A. Hamilton. 2020. The importance of quantitative trait differentiation in restoration: landscape heterogeneity and functional traits inform seed transfer guidelines. AoB Plants 12: plaa009.
Yoo, C. Y., H. E. Pence, J. B. Jin, K. Miura, M. J. Gosney, P. M. Hasegawa, and M. V Mickelbart. 2010. The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22: 4128-4141.
Young, A., T. Boyle, and T. Brown. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 11: 413-418.