Abstract
Phenotypic variation may be genetically determined or reflect phenotypic plasticity. More common plants are expected to be less differentiated between and within regions and more adapted than less common ones. However, such differences might not develop in hybridizing species which cannot evolve completely independently. We collected 311 genets of Carex flava, 215 of C. viridula and 46 of their hybrid C. × subviridula from 42 natural populations in cold temperate Estonia, mild temperate Lowland Switzerland and alpine Highland Switzerland. Three plantlets from each genet were planted to three experimental gardens, one in each region. We measured survival, growth, reproduction and morphological traits. The experimental transplants showed strong plasticity and grew smallest in the alpine garden. The less common C. viridula was slightly more differentiated between regions of origin than the more common C. flava and the hybrid. However, this depended on the experimental garden. Significant origin-by-garden-by-taxon and taxon-by-garden interactions suggest differential adaptation among populations and taxa. Regional differed from non-regional plants in several traits indicating both adaptations and, especially for C. viridula, maladaptations to the home regions. For C. flava, plant seed production was higher when mean annual temperature and precipitation were more similar between population of origin and garden, suggesting local adaptation to climate. Hybrids were intermediate between parental taxa or more similar to one of them, which was retained across gardens. We conclude that plasticity, genetic variation and genotype–environment interactions all contributed to regional differentiation of the closely related species. Hybridization did not completely align evolutionary patterns, and the less common species showed slightly more genetic differentiation between populations and more maladapted traits than the more common one.
This is a preview of subscription content, access via your institution.
References
Abbott RJ (2017) Plant speciation across environmental gradients and the occurrence and nature of hybrid zones. J Syst Evol 55:238–258. https://doi.org/10.1111/jse.12267
Anderson JT, Perera N, Chowdhury B, Mitchell-Olds T (2015) Microgeographic patterns of genetic divergence and adaptation across environmental gradients in Boechera stricta (Brassicaceae). Am Nat 186:S60–S73. https://doi.org/10.1086/682404
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Becker U, Colling G, Dostal P, Jakobsson A, Matthies D (2006) Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia 150:506–518. https://doi.org/10.1007/s00442-006-0534-9
Bischoff A, Müller-Schärer H (2010) Testing population differentiation in plant species—how important are environmental maternal effects. Oikos 119:445–454. https://doi.org/10.1111/j.1600-0706.2009.17776.x
Blackstock N, Ashton PA (2010) Genetic markers and morphometric analysis reveal past hybridization and introgression in putative Carex flava L. s. str. (Cyperaceae) hybrid populations. Plant Syst Evol 287:37–47. https://doi.org/10.1007/s00606-010-0287-0
Blanquart F, Gandon S, Nuismer SL (2012) The effects of migration and drift on local adaptation to a heterogeneous environment. J Evol Biol 25:1351–1363. https://doi.org/10.1111/j.1420-9101.2012.02524.x
Brennan AC, Hiscock SJ, Abbott RJ (2016) Genomic architecture of phenotypic divergence between two hybridizing plant species along an elevational gradient. AoB Plants 8:plw022. https://doi.org/10.1093/aobpla/plw022
Bucharova A, Michalski S, Hermann J-M, Heveling K, Durka W, Hölzel N, Kollmann J, Bossdorf O (2016) Genetic differentiation and regional adaptation among seed origins used for grassland restoration: lessons from a multispecies transplant experiment. J Appl Ecol 54:127–136. https://doi.org/10.1111/1365-2664.12645
Byars SG, Papst W, Hoffmann AA (2007) Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evolution 61:2925–2941. https://doi.org/10.1111/j.1558-5646.2007.00248.x
Campbell DR, Waser NM (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676. https://doi.org/10.1554/0014-3820(2001)055%5B0669:GBEIAT%5D2.0.CO;2
Clevering OA, Brix H, Lukavská J (2001) Geographic variation in growth responses in Phragmites australis. Aquat Bot 69:89–108. https://doi.org/10.1016/S0304-3770(01)00132-2
Crins WJ, Ball PW (1989) Taxonomy of the Carex flava complex (Cyperaceae) in North America and northern Eurasia. II. Taxonomic treatment. Can J Bot 67:1048–1065. https://doi.org/10.1139/b89-138
Davies EW (1953) Notes on Carex flava and its allies. III. The taxonomy and morphology of the British representatives. Watsonia 3:74–79
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242. https://doi.org/10.1146/annurev.es.24.110193.001245
Emms SK, Arnold ML (1997) The effect of habitat on parental and hybrid fitness: transplant experiments with Louisiana irises. Evolution 51:1112–1119. https://doi.org/10.2307/2411040
Estonian Weather Service (2015) The Estonian weather service. https://www.ilmateenistus.ee. Accessed 3 Apr 2018
Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27. https://doi.org/10.18637/jss.v008.i15
Freeman DC, Miglia KJ, McArthur ED, Graham JH, Wang H (1999) Narrow hybrid zone between two subspecies of big sagebrush (Artemisia tridentata: Asteraceae). X. Performance in reciprocal transplant gardens. In: USDA forest service proceedings RMRS-P-11, pp 15–24
Galloway LF, Fenster CB (2000) Population differentiation in an annual legume: local adaptation. Evolution 54:1173–1181. https://doi.org/10.1554/0014-3820(2000)054%5B1173:PDIAAL%5D2.0.CO;2
Gonzalo-Turpin H, Hazard L (2009) Local adaptation occurs along altitudinal gradient despite the existence of gene flow in the alpine plant species Festuca eskia. J Ecol 97:742–751. https://doi.org/10.1111/j.1365-2745.2009.01509.x
Govindaraju DR (1988) Relationship between dispersal ability and levels of gene flow in plants. Oikos. https://doi.org/10.2307/3565978
Gugger S, Kesselring H, Stöcklin J, Hamann E (2015) Lower plasticity exhibited by high-versus mid-elevation species in their phenological responses to manipulated temperature and drought. Ann Bot 116:953–962. https://doi.org/10.1093/aob/mcv155
Hamann E, Scheepens JF, Kesselring H, Armbruster GFJ, Stöcklin J (2017) High intraspecific phenotypic variation, but little evidence for local adaptation in Geum reptans populations in the Central Swiss Alps. Alp Bot 127:121–132. https://doi.org/10.1007/s00035-017-0185-y
Hedrén M (2002) Patterns of allozyme and morphological differentiation in the Carex flava complex (Cyperaceae) in Fennoscandia. Nord J Bot 22:257–301. https://doi.org/10.1111/j.1756-1051.2002.tb01373.x
Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588. https://doi.org/10.1086/597611
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Janyszek M, Jagodziński AM, Janyszek S, Wrońska-Pilarek D (2008) Morphological variability of Carex spicata Huds. utricles among plant communities. Flora 203:386–395. https://doi.org/10.1016/j.flora.2007.06.007
Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60:1585–1595. https://doi.org/10.1554/05-680.1
Joshi J, Schmid B, Caldeira MC, Dimitrakopoulos PG, Good J, Harris R, Hector A, Huss-Danell K, Jumpponen A, Minns A (2001) Local adaptation enhances performance of common plant species. Ecol Lett 4:536–544. https://doi.org/10.1046/j.1461-0248.2001.00262.x
Kaplan Z (2002) Phenotypic plasticity in Potamogeton (Potamogetonaceae). Folia Geobot 37:141–170. https://doi.org/10.1007/BF02804229
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables. Springer, Berlin
Körner C (2016) Plant adaptation to cold climates. F1000Research. https://doi.org/10.12688/f1000research.9107.1
Koutecký P (2015) MorphoTools: a set of R functions for morphometric analysis. Plant Syst Evol 301:1115–1121. https://doi.org/10.1007/s00606-014-1153-2
Kuchel SD, Bruederle LP (2000) Allozyme data support a Eurasian origin for Carex viridula subsp. viridula var. viridula (Cyperaceae). Madroño 47:147–158
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest Package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PloS One 3:e4010. https://doi.org/10.1371/journal.pone.0004010
Maad J, Armbruster WS, Fenster CB (2013) Floral size variation in Campanula rotundifolia (Campanulaceae) along altitudinal gradients: patterns and possible selective mechanisms. Nord J Bot 31:361–371. https://doi.org/10.1111/j.1756-1051.2013.01766.x
Meteoswiss (2015) Federal office of meteorology and climatology. http://www.meteoswiss.admin.ch. Accessed 3 Apr 2018
Miglia KJ, McArthur ED, Moore WS, Wang H, Graham JH, Freeman D (2005) Nine-year reciprocal transplant experiment in the gardens of the basin and mountain big sagebrush (Artemisia tridentata: Asteraceae) hybrid zone of Salt Creek Canyon: the importance of multiple-year tracking of fitness. Biol J Linn Soc 86:213–225. https://doi.org/10.1111/j.1095-8312.2005.00534.x
Molina-Montenegro MA, Naya DE (2012) Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species. PloS One 7:1–8. https://doi.org/10.1371/journal.pone.0047620
Pykälä J, Toivonen H (1994) Taxonomy of the Carex flava complex (Cyperaceae) in Finland. Nord J Bot 14:173–191. https://doi.org/10.1111/j.1756-1051.1994.tb00583.x
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rice KJ, Knapp EE (2008) Effects of competition and life history stage on the expression of local adaptation in two native bunchgrasses. Restor Ecol 16:12–23. https://doi.org/10.1111/j.1526-100X.2007.00257.x
Rieseberg LH, Burke JM (2001) The biological reality of species: gene flow, selection, and collective evolution. Taxon. https://doi.org/10.2307/1224511
Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914. https://doi.org/10.1126/science.1137729
Santamaría L, Figuerola J, Pilon JJ, Mjelde M, Green AJ, Boer T, King RA, Gornall RJ (2003) Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 84:2454–2461. https://doi.org/10.1890/02-0431
Scheepens JF, Stöcklin J (2013) Flowering phenology and reproductive fitness along a mountain slope: maladaptive responses to transplantation to a warmer climate in Campanula thyrsoides. Oecologia 171:679–691. https://doi.org/10.1007/s00442-012-2582-7
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693. https://doi.org/10.1146/annurev.es.17.110186.003315
Schmid B (1981) Die Verbreitung der Artengruppe Carex flava L. s.l. in der Schweiz. Bot Helv 91:3–8
Schmid B (1982) Karyology and hydridization in the Carex flava complex in Switzerland. Feddes Repert 93:23–59. https://doi.org/10.1002/fedr.19820930103
Schmid B (1984) Life histories in clonal plants of the Carex flava group. J Ecol 72:93–114. https://doi.org/10.2307/2260008
Schmid B (1986) Patterns of variation and population structure in the Carex flava group. Symb Bot Upsal 27:113–126
Schmid B (1992) Phenotypic variation in plants. Evol Trends Plants 6:45–60
Schmidt L, Fischer M, Schmid B, Oja T (2017) Despite admixing two closely related Carex species differ in their regional morphological differentiation. Plant Syst Evol 7:901–914. https://doi.org/10.1007/s00606-017-1420-0
Schmidt L, Fischer M, Oja T (2018) Two closely related species differ in their regional genetic differentiation despite admixing. AoB Plants 10:1–17. https://doi.org/10.1093/aobpla/ply007
Seguí J, Lázaro A, Traveset A, Salgado-Luarte C, Gianoli E (2018) Phenotypic and reproductive responses of an Andean violet to environmental variation across an elevational gradient. Alp Bot 128:59–69. https://doi.org/10.1007/s00035-017-0195-9
Šťastná P, Klimešová J, Doležal J (2012) Altitudinal changes in the growth and allometry of Rumex alpinus. Alp Bot 122:35–44. https://doi.org/10.1007/s00035-012-0099-7
Stöcklin J, Kuss P, Pluess AR (2009) Genetic diversity, phenotypic variation and local adaptation in the alpine landscape: case studies with alpine plant species. Bot Helv 119:125–133. https://doi.org/10.1007/s00035-009-0065-1
Toom M, Liira J, Kull T (2016) Tarnad—the genus Carex in Estonia, (in Estonian), 1st edn. University of Tartu, Tartu
Trunschke J, Stöcklin J (2017) Plasticity of flower longevity in alpine plants is increased in populations from high elevation compared to low elevation populations. Alp Bot 127:41–51. https://doi.org/10.1007/s00035-016-0176-4
Vonk DH (1979) Biosystematic studies of the Carex flava complex I. Flowering. Plant Biol 28:1–20. https://doi.org/10.1111/j.1438-8677.1979.tb01153.x
Wang H, McArthur ED, Sanderson SC, Graham JH, Freeman DC (1997) Narrow hybrid zone between two subspecies of big sagebrush (Artemisia tridentata: Asteraceae). IV. Reciprocal transplant experiments. Evolution 51:95–102. https://doi.org/10.2307/2410963
Więcław H (2014) Carex flava agg. (section Ceratocystis, Cyperaceae) in Poland: taxonomy, morphological variation, and soil conditions. Biodivers Res Conserv 33:3–51. https://doi.org/10.2478/biorc-2014-0001
Acknowledgements
We are thankful to the team of the Alpine Botanical Garden Schynige Platte, assistants at the University of Zurich and laboratory technicians at the University of Tartu for looking after and taking care of plants in the experimental gardens. We are also grateful to numerous people from the University of Bern who helped in measuring the plants during the experiment.
Funding
The work was supported by the Estonian Ministry of Education and Research, institutional research funding (IUT 20-28, 20-29) and the European Union through the European Regional Development Fund (Centre of Excellence EcolChange).
Author information
Authors and Affiliations
Contributions
LS and MF conceived the paper with BS and TO. LS performed the analyses and wrote the manuscript under the guidance of MF and with critical reviews and contributions from all coauthors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schmidt, L., Schmid, B., Oja, T. et al. Genetic differentiation, phenotypic plasticity and adaptation in a hybridizing pair of a more common and a less common Carex species. Alp Botany 128, 149–167 (2018). https://doi.org/10.1007/s00035-018-0211-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-018-0211-8
Keywords
- Carex flava group
- Genotype-by-environment interaction
- Performance
- Regional adaptation
- Transplant experiment
- Variability