Evidence of artificial selection: are orchids in cultivation an effective <i>ex situ</i> conservation strategy?

Authors

  • Raymond L. Tremblay Department of Biology, University of Puerto Rico, Humacao campus, José E. Aguiar Aramburu, Carr. 908, Km 1.2, Humacao, Puerto Rico, PR, 00791.,University of Puerto Rico https://orcid.org/0000-0002-8588-4372
  • Paola A. Alicea-Roman Department of Biology, University of Puerto Rico, Humacao campus, José E. Aguiar Aramburu, Carr. 908, Km 1.2, Humacao, Puerto Rico, PR, 00791.,University of Puerto Rico https://orcid.org/0000-0002-2516-1893
  • Abimelys Anaya-Reyes Department of Biology, University of Puerto Rico, Humacao campus, José E. Aguiar Aramburu, Carr. 908, Km 1.2, Humacao, Puerto Rico, PR, 00791.,University of Puerto Rico https://orcid.org/0000-0003-1893-527X
  • Sean Duclerc-Rodas Department of Biology, University of Puerto Rico, Humacao campus, José E. Aguiar Aramburu, Carr. 908, Km 1.2, Humacao, Puerto Rico, PR, 00791.,University of Puerto Rico
  • Ivanellys Medina-Tirado Department of Biology, University of Puerto Rico, Humacao campus, José E. Aguiar Aramburu, Carr. 908, Km 1.2, Humacao, Puerto Rico, PR, 00791.,University of Puerto Rico https://orcid.org/0000-0003-2767-3048

DOI:

https://doi.org/10.15517/lank.v22i3.53443

Keywords:

American Orchid Society, evolution, in situ conservation, morphological variation, natural selection, phenotypic selection

Abstract

Artificial selection is the process by which humans change morphological and genetic characteristics of species through selection of “favored” characters. Although the gray literature suggests the process is occurring in orchids held in ex situ collections, there is limited evidence of this in the scientific literature. There is a perspective among growers that species (not hybrids) held in ex situ collections are potential sources of material for use in in situ re-establishment, however, this assumes that there has not been any artificial selection for morphological characters, or functional traits while grown and propagated ex situ. Here we evaluate if plants grown in ex situ collections show changes in morphological characters across time and if the range of character size is within the range from in situ populations. We evaluated plants from the American Orchid Society database from nine genera and 54 species. We noted that 35% of characters evaluated had evidence of significant change across time. Moreover, for most species in ex situ the evaluated characters were frequently (95%) outside the range of plants of natural populations based on species descriptions. If variation in size of ex situ collections as compared to in situ plants is genetically based, it is possible that these would be functionally maladaptive if re-introduced to their natural environment. Protocols for ex situ conservation programs need to focus on the morphological, biochemical, and ecological interactions and genetic diversity that would render the re-introduction of ex situ to their natural environment to maximize the likelihood of effective re-establishment. Consequently, species which are awarded recognition at orchid shows may potentially be inappropriate for plants within an in situ reintroduction conservation program.

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References

Abeli, T., Dalrymple, S., Godefroid, S., Mondoni, A., Müller, J. V., Rossi, G. & Orsenigo, S. (2019). Ex situ collections and their potential for the restoration of extinct plants. Conservation Biology, 34(2), 303–313. doi: https://doi.org/10.1111/cobi.13391

Ackerman, J. D. and collaborators (2014). Orchid flora of the Greater Antilles. New York Botanical Garden Press.

Aggarwal, S. & Zettler, L. W. (2010). Reintroduction of an endangered terrestrial orchid, Dactylorhiza hatagirea (D.Don) Soo, assisted by symbiotic seed germination: First report from the Indian subcontinent. Nature and Science, 8(10), 139–145.

Abreu, P. P., Souza, M. M., Santos, E. A., Pires, M. V., Pires, M. M. & de Almeida, A. A. F. (2009). Passion flower hybrids and their use in the ornamental plant market: perspectives for sustainable development with emphasis on Brazil. Euphytica, 166, 307–315. doi: https://doi.org/10.1007/s10681-008-9835-x

Arnold, P. A., Kruuk, L. E. & Nicotra, A. B. (2019). How to analyse plant phenotypic plasticity in response to a changing climate. New Phytologist, 222(3), 1235–1241. doi: https://doi.org/10.1111/nph.15656

Basey, A. C., Fant, J. B. & Kramer, A. T. (2015). Producing native plant materials for restoration: 10 rules to collect and maintain genetic diversity. Native Plants Journal, 16(1), 37–53. doi: 10.3368/npj.16.1.37

Bateman, R. M. & Rudall, P. J. (2006). Evolutionary and morphometric implications of morphological variation among flowers within an inflorescence: a case-study using European orchids. Annals of Botany, 98(5), 975–993. doi: https://doi.org/10.1093/aob/mcl191

Benitez‐Vieyra, S., Medina, A. M., Glinos, E. & Cocucci, A. A. (2006). Pollinator-mediated selection on floral traits and size of floral display in Cyclopogon elatus, a sweat bee-pollinated orchid. Functional Ecology, 20(6), 948–957. doi: https://doi.org/10.1111/j.1365-2435.2006.01179.x

Benitez‐Vieyra, S., Medina, A. M. & Cocucci, A. A. (2009). Variable selection patterns on the labellum shape of Geoblasta pennicillata, a sexually deceptive orchid. Journal of Evolutionary Biology, 22(11), 2354–2362. doi: https://doi.org/10.1111/j.1420-9101.2009.01840.x

BFG (The Brazil Flora Group). (2021). Coleção Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. doi: https://doi.org/10.47871/jbrj2021004

Blinova, I. V. (2012). Intra-and interspecific morphological variation of some European terrestrial orchids along a latitudinal gradient. Russian Journal of Ecology, 43(2), 111–116. doi: https://doi.org/10.1134/S1067413612020051

Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Advances in genetics, 13, 115–155. doi: https://doi.org/10.1016/S0065-2660(08)60048-6

Budd, G. E. (2006). On the origin and evolution of major morphological characters. Biological Reviews, 81(4), 609–628. doi: 10.1017/S1464793106007135

Callahan, H. S. (2005). Using artificial selection to understand plastic plant phenotypes. Integrative and Comparative Biology, 45(3), 475–485. doi: https://doi.org/10.1093/icb/45.3.475

Calvo, R. N. (1993). Evolutionary demography of orchids: intensity and frequency of pollination and the cost of fruiting. Ecology, 74(4), 1033–1042. doi: https://doi.org/10.2307/1940473

Cameron, A. C. & Trivedi, P. K. (1998). Regression Analysis of Count Data. New York: Cambridge Press.

Cantarel, A. A., Allard, V., Andrieu, B., Barot, S., Enjalbert, J., Gervaix, J., Goldringer, I., Pommier, T., Saint-Jean, S. & Le Roux, X. (2021). Plant functional trait variability and trait syndromes among wheat varieties: the footprint of artificial selection. Journal of Experimental Botany, 72(4), 1166–1180. doi: https://doi.org/10.1093/jxb/eraa491

Casas, A., Otero-Arnaiz, A., Pérez-Negrón, E. & Valiente-Banuet, A. (2007). In situ management and domestication of plants in Mesoamerica. Annals of Botany, 100(5), 1101–1115. doi: https://doi.org/10.1093/aob/mcm126

Cavanaugh, J. E. & Neath, A. A. (2019). The Akaike information criterion: Background, derivation, properties, application, interpretation, and refinements. Wiley Interdisciplinary Reviews: Computational Statistics, 11(3), 1–11. doi: https://doi.org/10.1002/wics.1460

Chan, K. M., Pringle, R. M., Ranganathan, J., Boggs, C. L., Chan, Y. L., Ehrlich, P. R., Haff, P. K., Heller, N. E., Al-Khafaji, K. & Macmynowski, D. P. (2007). When agendas collide: human welfare and biological conservation. Conservation biology, 21(1), 59–68. doi: https://doi.org/10.1111/j.1523-1739.2006.00570.x

Charpulat, E., Le Roncé, I., Ågren, J. & Sletvold, N. (2020). Divergent selection on flowering phenology but not on floral morphology between two closely related orchids. Ecology and Evolution, 10(12), 5737–5747. doi: https://doi.org/10.1002/ece3.6312

Cibrian-Jaramillo, A., Hird, A., Oleas, N., Ma, H., Meerow, A. W., Francisco-Ortega, J. & Griffith, M. P. (2013). What is the conservation value of a plant in a botanic garden? Using indicators to improve management of ex situ collections. The Botanical Review, 79, 559–577. doi: https://doi.org/10.1007/s12229-013-9120-0

Cintrón-Berdecía, S. T. & Tremblay, R. L. (2006). Spatial variation in phenotypic selection on floral characteristics in an epiphytic orchid. Folia Geobotanica, 41, 33–46. doi: https://doi.org/10.1007/BF02805260

Conner, J. K. (2003). Artificial selection: a powerful tool for ecologists. Ecology, 84(7), 1650–1660. doi: https://doi.org/10.1890/0012-9658(2003)084[1650:ASAPTF]2.0.CO;2

Cribb, P. (1987). The Genus Paphiopedilum. Kota Kinabalu: Natural History Publications (Borneo) in association with Royal Botanic Gardens Kew, 1998.

Crow, E. L. & Shimizu, K. (1987). Lognormal distributions. New York: Marcel Dekker.

Curio, E. (1996). Conservation needs ethology. Trends in Ecology & Evolution, 11(6), 260–263. doi: https://doi.org/10.1016/0169-5347(96)20046-1

de Jager, M. L. & Peakall, R. (2019). Experimental examination of pollinator-mediated selection in a sexually deceptive orchid. Annals of Botany, 123(2), 347–354. doi: https://doi.org/10.1093/aob/mcy083

Datta, S. K. (2021). Breeding of ornamentals: success and technological status. The Nucleus, 65, 107–128. doi: https://doi.org/10.1007/s13237-021-00368-x

Darwin, C. (1877). The various contrivances by which orchids are fertilised by insects. London: John Murray, Albemarle Street.

Das, M. C., Devi, S. D., Kumaria, S. & Reed, B. M. (2021). Looking for a way forward for the cryopreservation of orchid diversity. Cryobiology, 102, 1–14. doi: https://doi.org/10.1016/j.cryobiol.2021.05.004

Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature, 418(6898), 700–707.

Dormont, L., Joffard, N. & Schatz, B. (2019). Intraspecific variation in floral color and odor in orchids. International Journal of Plant Sciences, 180(9), 1036–1058. doi: https://doi.org/10.1086/705589

Endler, J. A. (1986). Natural Selection in the Wild. Monograph in Population Biology, vol. 21, 1–354. Princeton University Press. https://doi.org/10.12987/9780691209517

Engels, J. M. M. & Ebert, A. W. (2021). A critical review of the current global ex situ conservation system for plant agrobiodiversity. I. History of the development of the global system in the context of the political/legal framework and its major conservation components. Plants, 10(8), 1557. doi: https://doi.org/10.3390/plants10081557

Ensslin, A., Tschöpe, O., Burkart, M. & Joshi, J. (2015). Fitness decline and adaptation to novel environments in ex situ plant collections: Current knowledge and future perspectives. Biological Conservation, 192, 394–401. doi: https://doi.org/10.1016/j.biocon.2015.10.012

Ensslin, A., Van de Vyver, A., Vanderborght, T. & Godefroid, S. (2018). Ex situ cultivation entails high risk of seed dormancy loss on short‐lived wild plant species. Journal of Applied Ecology, 55(3), 1145–1154. doi: https://doi.org/10.1111/1365-2664.13057

Evans, M. C. (2021). Re-conceptualizing the role(s) of science in biodiversity conservation. Environmental Conservation, 48(3), 151–160. doi: 10.1017/S0376892921000114

Ferson, S., & Burgman, M. (Eds.). (2006). Quantitative methods for conservation biology. Springer Science & Business Media.

Fiani, A., Pudjiono, S. & Hakim, L. (2021). Ex-situ conservation through selection and breeding: A Review On 15 Years Toona sinensis Roem. & Toona sureni Merr. base populations. IOP Conference Series: Earth and Environmental Science, 912(1), 1–8. doi: 10.1088/1755-1315/912/1/012034

Field, A., Miles, J. & Field, Z. (2012). Discovering Statistics using R. London, UK: Sage publications.

Firke S. (2021). janitor: Simple Tools for Examining and Cleaning Dirty Data. R package version 2.1.0. https://CRAN.R-project.org/package=janitor

Fujino, K., Kawahara, Y. & Shirasawa, K. (2021). Artificial selection in the expansion of rice cultivation. Theoretical and Applied Genetics, 135, 291–299. doi: https://doi.org/10.1007/s00122-021-03966-0

Gaskett, A. C. (2012). Floral shape mimicry and variation in sexually deceptive orchids with a shared pollinator. Biological Journal of the Linnean Society, 106(3), 469–481. doi: https://doi.org/10.1111/j.1095-8312.2012.01902.x

Griffith, M. P., Calonje, M., Meerow, A. W., Francisco-Ortega, J., Knowles, L., Aguilar, R., Tut, F., Sánchez, V., Meyer, A., Noblick, L. R. & Magellan, T. M. (2017). Will the same ex situ protocols give similar results for closely related species? Biodiversity and Conservation, 26(12), 2951–2966. doi: https://doi.org/10.1007/s10531-017-1400-2

Grolemund, G. & Wickham, H. (2011). Dates and Times Made Easy with lubridate. Journal of Statistical Software, 40(3), 1–25. doi: https://doi.org/10.18637/jss.v040.i03

Guerrant Jr, E. O., Havens, K. & Vitt, P. (2014). Sampling for effective ex situ plant conservation. International Journal of Plant Sciences, 175(1), 11–20. doi: https://doi.org/10.1086/674131

Hamelin, R. (2012). Phenotypic Selection and Maladaptation in Restored and Natural Tall Grass Prairie Populations of Monarda fistulosa. Doctoral dissertation, University of Guelph.

Havens, K., Guerrant Jr., E. O., Maunder, M. & Vitt, P. (2004). Guidelines for ex situ conservation collection management: minimizing risks, Appendix 3. In: E. O. Guerrant Jr., K. Havens & M. Maunder (Eds.), Ex situ plant conservation: supporting species survival in the wild (pp. 454–473). Island Press.

Havens, K., Vitt, P., Maunder, M., Guerrant, E. O. & Dixon, K. (2006). Ex situ plant conservation and beyond. BioScience, 56(6), 525–531. doi: https://doi.org/10.1641/0006-3568(2006)56[525:ESPCAB]2.0.CO;2

Hay, F. R., Whitehouse, K. J., Ellis, R. H., Hamilton, N. R. S., Lusty, C., Ndjiondjop, M. N., Tia, D., Wenzl, P., Santos, L. G., Yazbek, M. & Azevedo, V.C. (2021). CGIAR genebank viability data reveal inconsistencies in seed collection management. Global Food Security, 30, 100557.

Hilbe, J. M. (2011). Negative binomial regression. Cambridge, UK: Cambridge University Press.

Hinsley, A., de Boer, H. J., Fay, M. F., Gale, S. W., Gardiner, L. M., Gunasekara, R. S., Kumar, P., Masters, S., Metusala, D., Roberts, D. L., Veldman, S., Wong, S. & Phelps, J. (2018). A review of the trade in orchids and its implications for conservation. Botanical Journal of the Linnean Society, 186(4), 435–455. doi: https://doi.org/10.1093/botlinnean/box083

Hugh-Jones, D. (2021). huxtable: Easily Create and Style Tables for LaTeX, HTML and Other Formats. R package version 5.4.0. https://CRAN.R-project.org/package=huxtable

Jiménez, R., Peláez, R., González, R., Hágsater, E., Soto, M. & Halbinger, F. (1997). Laelias of Mexico. Mexico City: Herba-rio Amo.

Juillet, N. & Scopece, G. (2010). Does floral trait variability enhance reproductive success in deceptive orchids? Perspectives in Plant Ecology, Evolution and Systematics, 12(4), 317–322. doi: https://doi.org/10.1016/j.ppees.2010.05.001

Kabacoff, R. I. (2015). R in action: data analysis and graphics with R. Simon and Schuster.

Kassambara, A. (2021). Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R package version 0.7.0. https://CRAN.R-project.org/package=rstatix

Kaur, S. (2019). Cryopreservation of Orchids–A Review. Recent Patents on Biotechnology, 13(2), 114–123. doi: https://doi.org/10.2174/1872208313666181127143058

Kim, Y. K., Kang, K. W. & Kim, K. J. (2016). Restoration of endangered orchid species, Dendrobium moniliforme (L.) Sw. (Orchidaceae) in Korea. Korean Journal of Plant Taxonomy, 46(2), 256–266. doi: https://doi.org/10.11110/kjpt.2016.46.2.256

Li, D. Z. & Pritchard, H. W. (2009). The science and economics of ex situ plant conservation. Trends in plant science, 14(11), 614–621. doi: https://doi.org/10.1016/j.tplants.2009.09.005

Li, C., Dong, N., Zhao, Y., Wu, S., Liu, Z. & Zhai, J. (2021). A Review for the Breeding of Orchids: Current Achievements and Prospects. Horticultural Plant Journal, 7(5), 380–392. doi: https://doi.org/10.1016/j.hpj.2021.02.006

Kluge, M., Razanoelisoa, B. & Brulfert, J. (2001). Implications of genotypic diversity and phenotypic plasticity in the ecophysiological success of CAM plants, examined by studies on the vegetation of Madagascar. Plant Biology, 3(3), 214–222. doi: 10.1055/s-2001-15197

Lofflin, D. L. & Kephart, S. R. (2005). Outbreeding, seedling establishment, and maladaptation in natural and reintroduced populations of rare and common Silene douglasii (Caryophyllaceae). American Journal of Botany, 92(10), 1691–1700. doi: https://doi.org/10.3732/ajb.92.10.1691

Maad, J. (2000). Phenotypic selection in hawkmoth‐pollinated Platanthera bifolia: targets and fitness surfaces. Evolution, 54(1), 112–123. doi: https://doi.org/10.1111/j.0014-3820.2000.tb00012.x

Marasek-Ciolakowska, A., Sochacki, D. & Marciniak, P. (2021). Breeding aspects of selected ornamental bulbous crops. Agronomy, 11(9), 1709. doi: https://doi.org/10.3390/agronomy11091709

Montalvo, A. M. & Ackerman, J. D. (1987). Limitations to fruit production in Ionopsis utricularioides (Orchidaceae). Biotropica, 19(1), 24–31. doi: https://doi.org/10.2307/2388456

Moré, M., Amorim, F. W., Benitez-Vieyra, S., Medina, A. M., Sazima, M. & Cocucci, A. A. (2012). Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids. PLoS One, 7(7), e41878. doi: https://doi.org/10.1371/journal.pone.0041878

Murren, C. J., Auld, J. R., Callahan, H., Ghalambor, C. K., Handelsman, C. A., Heskel, M. A., Kingsolver, J. G., Maclean, H. J., Masel, J., Maughan, H., Pfennig, D. W., Relyea, R. A., Seiter, S., Snell-Rood, E., Steiner, U. K. & Schlichting, C. D. (2015). Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity, 115(4), 293–301. doi: https://doi.org/10.1038/hdy.2015.8

Newman, S. A. & Müller, G. B. (2000). Epigenetic mechanisms of character origination. Journal of Experimental Zoology, 288(4), 304–317.

Obeso, J. R. (2002). The costs of reproduction in plants. New phytologist, 155(3), 321–348. doi: 10.1046/j.1469-8137.2002.00477.x

Palacio, F. X., Ordano, M. & Benitez-Vieyra, S. (2019). Measuring natural selection on multivariate phenotypic traits: a protocol for verifiable and reproducible analyses of natural selection. Israel Journal of Ecology and Evolution, 65(3–4), 130–136. doi: https://doi.org/10.1163/22244662-20191064

Phartyal, S. S., Thapliyal, R. C., Koedam, N., & Godefroid, S. (2002). Ex situ conservation of rare and valuable forest tree species through seed-gene bank. Current Science, 1351–1357.

Pigliucci, M. (2005). Evolution of phenotypic plasticity: where are we going now? Trends in ecology & evolution, 20(9), 481–486. doi: https://doi.org/10.1016/j.tree.2005.06.001

Phillips, R. D., Reiter, N. & Peakall, R. (2020). Orchid conservation: from theory to practice. Annals of Botany, 126(3), 345–362. doi: https://doi.org/10.1093/aob/mcaa093

Rauschkolb, R., Szczeparska, L., Kehl, A., Bossdorf, O. & Scheepens, J. F. (2019). Plant populations of three threatened species experience rapid evolution under ex situ cultivation. Biodiversity and Conservation, 28(14), 3951–3969.

Rebeiz, M. & Tsiantis, M. (2017). Enhancer evolution and the origins of morphological novelty. Current Opinion in Genetics & Development, 45, 115–123. doi: https://doi.org/10.1016/j.gde.2017.04.006

Salazar-Ciudad, I. (2007). On the origins of morphological variation, canalization, robustness, and evolvability. Integrati-ve and Comparative Biology, 47(3), 390–400.

Salazar-Rojas, V. M., Herrera-Cabrera, B. E., Delgado-Alvarado, A., Soto-Hernández, M., Castillo-González & Cobos-Peralta, M. (2012). Chemotypical variation in Vanilla planifolia Jack. (Orchidaceae) from the Puebla-Veracruz Totonacapan region. Genetic Resources and Crop Evolution, 59, 875–887. doi: https://doi.org/10.1007/s10722-011-9729-y.

Seaton, P. T. (2007). Establishing a global network of orchid seed banks. Lankesteriana, 7, 371–375. https://doi.org/10.15517/lank.v7i1-2.19567.

Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in ecology & evolution, 19(4), 198–207. doi: https://doi.org/10.1016/j.tree.2004.01.003

Shepard, K. A. & Purugganan, M. D. (2002). The genetics of plant morphological evolution. Current opinion in plant biology, 5(1), 49–55. doi: https://doi.org/10.1016/S1369-5266(01)00227-8

Scopece, G., Juillet, N., Lexer, C. & Cozzolino, S. (2017). Fluctuating selection across years and phenotypic variation in food-deceptive orchids. PeerJ, 5(3704). doi: https://doi.org/10.7717/peerj.3704

Shi, W., Pan, B., Gaskin, J. F. & Kang, X. (2009). Morphological variation and chromosome studies in Calligonum mongolicum and C. pumilum (Polygonaceae) suggests the presence of only one species. Nordic Journal of Botany, 27(2), 81–85. doi: 10.1111/j.1756-1051.2008.00338.x

Shirey, P. D., Kunycky, B. N., Chaloner, D. T., Brueseke, M. A. & Lamberti, G. A. (2013). Commercial trade of federally listed threatened and endangered plants in the United States. Conservation Letters, 6(5), 300–316.

Snell‐Rood, E. C., Van Dyken, J. D., Cruickshank, T., Wade, M. J. & Moczek, A. P. (2010). Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. Bioessays, 32(1), 71–81. doi: 10.1002/bies.200900132

Su, S., Shao, X., Zhu, C., Xu, J., Lu, H., Tang, Y., Jiao, K., Guo, W., Xiao, W., Liu, Z., Luo, D. & Huang, X. (2018). Transcriptome-wide analysis reveals the origin of peloria in Chinese Cymbidium (Cymbidium sinense). Plant and Cell Physiology, 59(10), 2064–2074. doi: https://doi.org/10.1093/pcp/pcy130

Swarts, N. D. & Dixon, K. W. (2009). Terrestrial orchid conservation in the age of extinction. Annals of botany, 104(3), 543–556. doi: https://doi.org/10.1093/aob/mcp025

Swarts, N. D. & Dixon, K. W. (2017). Conservation methods for terrestrial orchids. United States: J. Ross Publishing.

Sweet, H. R. (1980). The Genus Phalaenopsis. The Orchid Digest. Inc., Pomona, California.

Tremblay, R. L. (1992). Trends in the pollination ecology of the Orchidaceae: evolution and systematics. Canadian Journal of Botany, 70(3), 642–650. doi: https://doi.org/10.1139/b92-083

Tremblay 1997

Tremblay, R. L. (2005). Larger is better: the effect of floral display on reproductive success in two populations of Caladenia (Stegostyla) gracilis R. Br. Muelleria, 22, 77–85.

Tremblay, R. L. (2006). The effect of flower position on male and female reproductive success in a deceptively pollinated tropical orchid. Botanical Journal of the Linnean Society, 151(3), 405–410. doi: https://doi.org/10.1111/j.1095-8339.2006.00504.x

Tremblay, R. L. & Ackerman, J. D. (2001). Gene flow and effective population size in Lepanthes (Orchidaceae): a case for genetic drift. Biological Journal of the Linnean Society, 72(1), 47–62. doi: https://doi.org/10.1111/j.1095-8312.2001.tb01300.x

Tremblay, R. L., Ackerman, J. D. & Pérez, M. E. (2010). Riding across the selection landscape: fitness consequences of annual variation in reproductive characteristics. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1539), 491–498. doi: https://doi.org/10.1098/rstb.2009.0239

Tremblay, R. L., Ackerman, J. D., Zimmerman, J. K. & Calvo, R. N. (2005). Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society, 84(1), 1–54. doi: https://doi.org/10.1111/j.1095-8312.2004.00400.x

Tremblay, R. L. & Bould, A. (2017). Extraordinary variation in vegetation and floral characteristics among years in a terrestrial herb, Case Study 2.1. In N. D. Swarts & K. W. Dixon, Conservation methods for terrestrial orchids. J. Ross Publishing.

Trunschke, J. (2018). Pollinator-mediated selection and the evolution of floral traits in orchids (Doctoral dissertation, Acta Universitatis Upsaliensis).

Wei, X. & Jiang, M. (2021). Meta‐analysis of genetic representativeness of plant populations under ex situ conservation in contrast to wild source populations. Conservation Biology, 35(1), 12–23. doi: 10.1111/cobi.13617

Van Tassel, D. L., DeHaan, L. R. & Cox, T. S. (2010). Missing domesticated plant forms: can artificial selection fill the gap? Evolutionary Applications, 3(5–6), 434–452. doi: 10.1111/j.1752-4571.2010.00132.x

van den Berg, C. (2021). BFG. The Brazil Flora Group. 2021. Coleção Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Rio de Janeiro. pp.1–200. https://doi.org/10.47871/jbrj2021004

Vitt, P., Havens, K., Guerrant, E. O., & Maunder, M. (2004). Integrating quantitative genetics into ex situ conservation and restoration practices. In Ex situ plant conservation: supporting species survival in the wild (pp. 286-304). Island Press.

Volis, S. & Blecher, M. (2010). Quasi in situ: a bridge between ex situ and in situ conservation of plants. Biodiversity and conservation, 19(9), 2441–2454. doi: https://doi.org/10.1007/s10531-010-9849-2

Volis, S., Blecher, M. & Sapir, Y. (2009). Complex ex situ-in situ approach for conservation of endangered plant species and its application to Iris atrofusca of the Northern Negev. BioRisk, 3, 137–160. doi: 10.3897/biorisk.3.5

Wang, S., Xiao, Z., Yang, T., Jiang, M. & Wei, X. (2021). Shifts in leaf herbivory stress and defense strategies of endangered tree species after 20–35 years of ex-situ conservation. Global Ecology and Conservation, 26, 1–11. doi: https://doi.org/10.1016/j.gecco.2021.e01490

Warnes, G. R., Bolker, B., Lumley, T. & Johnson, R. C. (2018). gmodels: Various R Programming Tools for Model Fitting. R package version 2.18.1. https://CRAN.R-project.org/package=gmodels.

Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.

Wickham, H. (2019). stringr: Simple, Consistent Wrappers for Common String Operations. R package version 1.4.0. https://CRAN.R-project.org/package=stringr.

Wickham, H., François, R., Henry, L. & Müller, K. (2022). dplyr: A Grammar of Data Manipulation. R package version 1.0.8. https://CRAN.R-project.org/package=dplyr.

Zhao, D. K., Selosse, M. A., Wu, L., Luo, Y., Shao, S. C. & Ruan, Y. L. (2021). Orchid Reintroduction Based on Seed Germination-Promoting Mycorrhizal Fungi Derived From Protocorms or Seedlings. Frontiers in plant science, 12, 701152. doi: https://doi.org/10.3389/fpls.2021.701152

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Published

2022-12-14

How to Cite

Tremblay, R. L., Alicea-Roman, P. A., Anaya-Reyes, A., Duclerc-Rodas, S., & Medina-Tirado, I. (2022). Evidence of artificial selection: are orchids in cultivation an effective &lt;i&gt;ex situ&lt;/i&gt; conservation strategy?. Lankesteriana: International Journal on Orchidology, 22(3). https://doi.org/10.15517/lank.v22i3.53443

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