Abstract
Habitat differences might promote adaptive differentiation among populations that can be evidenced by genotype-by-environment interactions (GxE). I examined GxE in seed germination and seedling survival in demes of a rainforest cycad across their native and degraded-forest habitats, and explored the role of maternal effects and resource availability on the observed GxE. A reciprocal-transplant experiment showed a home-site advantage in terms of establishmen of the demes. Germination in a manipulative greenhouse experiment mirrored the patterns in natural environments, with GxE in response to light and water availability. Overall germination was lower in the degraded-forest habitat and under high-light and low-water conditions in the greenhouse. Several analysis suggested that maternal effects related to size on germination are weak, but maternal effects are suggested by better survival of larger seedlings in the degraded-forest habitat. With weak maternal effects, GxE in establishment of individuals suggest some adaptive differentiation across demes in this cycad, which could have implications for population persistence in its habitats.
Resumen
Diferencias entre habitats pueden resultar en divergencia adaptativa entre poblaciones que se evidencia por interacciones genotipo-ambiente (GxA). Examiné GxA en germinación y supervivencia de plántulas en demes de una cycada de bosques tropicales en sus habitats de bosques nativos y degradados, y exploré el papel de efectos maternos y disponibilidad de recursos en las GxA observadas. Un experimento de transplante recíproco mostró una ventaja de sitio nativo en términos de establecimiento para los demes. La germinación en un experimento de invernadero simuló los patrones en ambientes naturales, con GxA en respuesta a la disponibilidad de luz y humedad. En general la germinación fue mas baja en el habitat de bosque degradado y en las condiciones de alta luz y baja humedad en el invernadero. Varios análisis sugirieron que los efectos maternos relacionados con el tamaño sobre la germinación son débiles, pero efectos maternos podrían existir dada una mejor supervivencia de plántulas de mayor tamaño en el habitat de bosque degradado. Con efectos maternos débiles, GxA en el establecimiento de individuos sugieren algún grado de divergencia adaptativa entre demes de esta cycada, lo cual podría tener implicaciones para la persistencia de las poblaciones en sus habitats.
Similar content being viewed by others
Literature Cited
Aldrich, P. R., J. L. Hamrick, P. Chavarriaga & G. Kochert. 1998. Microsatellite analysis of demographic genetic structure in fragmented populations of the tropical tree Symphonia globulifera. Molecular Ecology 7: 933–944.
Andalo, C., S. J. Mazer, B. Godelle & N. Machon. 1999. Parental environmental effects on life history traits in Arabidopsis thaliana (Brassicaceae). New Phytologist 142: 173–184.
Antonovics, J., A. D. Bradshaw & R. G. Turner. 1971. Heavy metal tolerance in plants. Advanced Ecological Research 7: 1–85.
Becker, U., G. Colling, P. Dostal, A. Jakobsson & D. Matthies. 2006. Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia 150: 506–518.
Bischoff, A., L. Cremieux, M. Smilauerova, C. S. Lawson, S. R. Mortimer, J. Dolezal, V. Lanta, A. R. Edwards, A. J. Brook, M. Macel, J. Leps, T. Steinger & H. Muller-Scharer. 2006. Detecting local adaptation in widespread grassland species - the importance of scale and local plant community. Journal of Ecology 94: 1130–1142.
Bone, E. & A. Farres. 2001. Trends and rates of microevolution in plants. Genetica 112–113: 165–182.
Bonfil, C. 1998. The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae). American Journal of Botany 85: 79–87.
Bruna, E. M. 2002. Effects of forest fragmentation on Heliconia acuminata seedling recruitment in central Amazonia. Oecologia 132: 235–243.
Byars, S. G., W. Papst & A. A. Hoffmann. 2007. Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evolution 61: 2925–2941.
Campbell, D. R. 1997. Genetic and environmental variation in life-history traits of a monocarpic perennial: a decade-long field experiment. Evolution 51: 373–382.
Castro, J. 1999. Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytologist 144: 153–161.
Crandall, K. A., R. P. O. Bininda-Emos, G. M. Mace & R. K. Wayne. 2000. Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution 15: 290–295.
Daws, M. I., N. C. Garwood & H. W. Pritchard. 2005. Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panama: some ecological implications. Functional Ecology 19: 874–885.
Donaldson, J. S. 2003. Status Survey and Conservation Action plan: Cycads. IUCN/SSC Cycads Specialist Group. IUCN, Glan. 86.
Donohue, K., L. Dorn, C. Griffith, E. Kim, A. Aguilera, C. R. Polisetty & J. Schmitt. 2005. Environmental and genetic influences on the germination of Arabidopsis thaliana in the field. Evolution 59: 740–757.
Ellis, A. G. & A. E. Weis. 2006. Coexistence and differentiation of ‘flowering stones’: the role of local adaptation to soil microenvironment. Journal of Ecology 94: 322–335.
Engelbrecht, B. M. J. & T. A. Kursar. 2003. Comparative drought-resistance of seedlings of 28 species of co-ocurring tropical woody plants. Oecologia 136: 383–393.
Eriksson, O. 1999. Seed size variation and its effect on germination and seedling performance in the clonal herb Convallaria majalis. Acta Oecologica-International Journal of Ecology 20: 61–66.
Everham, E. M., R. W. Myster & E. VandeGenachte. 1996. Effects of light, moisture, temperature, and litter on the regeneration of five tree species in the tropical montane wet forest of Puerto Rico. American Journal of Botany 83: 1063–1068.
Farnsworth, E. 2000. The ecology and physiology of viviparous and recalcitrant seeds. Annual Review of Ecology and Systematics 31: 107–138.
Farnsworth, E. J. & J. M. Farrant. 1998. Reductions in abscisic acid are linked with viviparous reproduction in mangroves. American Journal of Botany 85: 760–769.
Finch-Savage, W. E. & H. A. Clay. 1994. Evidence that ethylene, light and abscisic acid interact to inhibit germination in the recalcitrant seeds of Quercus robur L. Journal of Experimental Botany 45: 1295–1299.
Fisher, B. L., H. F. Howe & S. J. Wright. 1991. Survival and growth of Virola surinamensis yearling: water augmentation in gap and understory. Oecologia 86: 292–297.
Galloway, L. F. 1995. Response to natural environmental heterogeneity: maternal effects and selection on life-history characters and plasticities in Mimulus guttatus. Evolution 49: 1095–1107.
——— 2001. Parental environmental effects on life history in the herbaceous plant Campanula americana. Ecology 82: 2781–2789.
——— 2005. Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytologist 166: 93–100.
Garwood, N. C. 1983. Seed germination in a seasonal tropical forest in Panama: a communit study. Ecological Monographs 53: 159–181.
Gomez, L. D. 1982. Plantae Mesoamericanae novae II. Phytologia 50: 401–404.
Herrera, C. M. 2000. Individual differences in progeny viability in Lavandula latifolia: a long-term field study. Ecology 81: 3036–3047.
Hufford, K. M. & S. J. Mazer. 2003. Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution 18: 147–155.
Janzen, F. J. & H. S. Stern. 1998. Logistic regression for empirical studies of multivariate selection. Evolution 52: 1564–1571.
Kang, H., G. Jaschek & K. S. Bawa. 1992. Variation in seed and seedling traits in Pithecellobium pedicellare, a tropical rain-forest tree. Oecologia 91: 239–244.
Kawecki, T. J. & D. Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225–1241.
Kirkpatrick, M. & R. Lande. 1989. The evolution of maternal characters. Evolution 43: 485–503.
Kyereh, B., M. D. Swaine & J. Thompson. 1999. Effect of light on the germination of forest trees in Ghana. Journal of Ecology 87: 772–783.
Latta, R. G., J. L. Mackenzie, A. Vats & D. J. Schoen. 2004. Divergence and variation of quantitative traits between allozyme genotypes of Avena barbata from contrasting habitats. Journal of Ecology 92: 57–71.
Linhart, Y. B. & M. C. Grant. 1996. Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27: 237–277.
Lopez-Gallego, C. 2007. Effects of habitat degradation on the evolutionary dynamics of populations in a rainforest cycad (Gymnospermae). Dept. of Biology, University of New Orleans, New Orleans.
——— & P. O’Neil. 2010. Life-history variation following habitat degradation associated with differing fine-scale spatial genetic structure in a rainforest cycad. Population Ecology 52: 191–201.
Lowe, A. J., D. Boshier, M. Ward, C. F. E. Bacles & C. Navarro. 2005. Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95: 255–273.
Luzuriaga, A. L., A. Escudero & F. Perez-Garcia. 2006. Environmental maternal effects on seed morphology and germination in Sinapis arvensis (Cruciferae). Weed Research 46: 163–174.
Macel, M., C. S. Lawson, S. R. Mortimer, M. Smilauerova, A. Bischoff, L. Cremieux, J. Dolezal, A. R. Edwards, V. Lanta, T. M. Bezemer, W. H. van der Putten, J. M. Igual, C. Rodriguez-Barrueco, H. Muller-Scharer & T. Steinger. 2007. Climate vs. soil factors in local adaptation of two common plant species. Ecology 88: 424–433.
Mathews, S. 2006. Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Molecular Ecology 15: 3483–3503.
Mazer, S. J. & D. L. Gorchov. 1996. Parental effects on progeny phenotype in plants: distinguishing genetic and environmental causes. Evolution 50: 44–53.
——— & C. T. Schick. 1991. Constancy of population parameters for life history and floral traits in Raphanus sativus L. I. Norms of reaction and the nature of genotype by environment interactions. Heredity 67: 143–156.
Moritz, C. 1994. Defining “Evolutionary Significant Units” for conservation. Trends in Ecology and Evolution 9: 373–375.
Munir, J., L. A. Dorn, K. Donohue & J. Schmitt. 2001. The effect of maternal photoperiod on seasonal dormancy in Arabidopsis thaliana (Brassicaceae). American Journal of Botany 88: 1240–1249.
Noble, I. R. & R. Dirzo. 1997. Forest as human-dominated ecosystems. Science 277: 522–525.
Norstog, K. J. & T. J. Nicholls. 1997. The biology of the Cycads. Cornell University Press, Ithaca.
Pammenter, N. W. & P. Berjak. 2000. Evolutionary and ecological aspects of recalcitrant seed biology. Seed Science Research 10: 301–306.
Paz, H., S. J. Mazer & M. Martinez-Ramos. 1999. Seed mass, seedling emergence, and environmental factors in seven rain forest Psychotria (Rubiaceae). Ecology 80: 1594–1606.
Peroni, P. A. 1995. Field and laboratory investigations of seed dormancy in red maple (Acer rubrum L.) from the North Carolina piedmont. Forest Science 41: 378–386.
Petit, R. J. & A. Hampe. 2006. Some evolutionary consequences of being a tree. Annual Review of Ecology and Systematics 37: 187–214.
Raich, J. W. & G. W. Khoon. 1990. Effects of canopy openings on tree seed-germination in a Malaysian dipterocarp forest. Journal of Tropical Ecology 6: 203–217.
Rasband, W. S. 2012. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997–2012.
Rice, K. J., D. R. Gordon, J. L. Hardinson & J. M. Welker. 1993. Phenotypic variation in seedling of a keystone tree species (Quercus douglasii) - The interactive effects of acorn source and competitive environment. Oecologia 96: 537–547.
Schmitt, J., J. Niles & R. D. Wulff. 1992. Norms of Reaction of seed traits to maternal environments in Plantago lanceolata. American Naturalist 139: 451–466.
Seiwa, K. 2000. Effects of seed size and emergence time on tree seedling establishment: importance of developmental constraints. Oecologia 123: 208–215.
Shaw, A. J. 1991. Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton.
Smith, T. B., M. W. Bruford & R. K. Wayne. 1993. The preservation of process: the missing element of conservation programs. Biodiversity Letters 1: 164–167.
SPSS Inc. 2009. PASW statistics for Windows, Version 18.0. Chicago: SPSS Inc.
Stockwell, C. A., A. P. Hendry & M. T. Kinnison. 2003. Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18: 94–101.
Sultan, S. 1996. Phenotypic plasticity for offspring traits in Polygonum persicaria. Ecology 77: 1791–1807.
——— 2004. Promising directions in plant phenotypic plasticity. Perspectives in Plan Ecology, Evolution and Systematics 6: 227–233.
Sultan, S. E. 2001. Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82: 328–343.
Tabarelli, M., M. J. C. Da Silva & C. Gascon. 2004. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodiversity and Conservation 13: 1419–1425.
Tang, W. 1990. Reproduction in the Cycad Zamia-Pumila in a Fire-Climax Habitat - an 8-Year Study. Bulletin of the Torrey Botanical Club 117: 368–374.
Tobin, M. F., O. R. Lopez & T. A. Kursar. 1999. Responses of tropical understory plants to a severe drought: Tolerance and avoidance of water stress. Biotropica 31: 570–578.
Turner, I. M. 1990. The seedling survivorship and growth of three Shorea species in a Malaysian tropical rain forest. Journal of Tropical Ecology 6: 469–478.
Tweddle, J. C., J. B. Dickie, C. C. Baskin & J. M. Baskin. 2003. Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91: 294–304.
Vazquez-Yanes, C. & A. Orozco-Segovia. 1993. Patterns of seed longevity and germination in the tropical rainforest. Annual Review of Ecology and Systematics 24: 69–87.
Wulff, R. D., A. Caceres & J. Schmitt. 1994. Seed and seedling responses to maternal and offspring environments in Plantago lanceolata. Functional Ecology 8: 763–769.
Acknowledgments
I thank the personnel at Corcovado National Park in Costa Rica for their help during fieldwork, and at Montgomery Botanical Center for support during the greenhouse experiment. This research was funded by a couple of research grants awarded to CLG by the Montgomery Botanical Center (FL, USA).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lopez-Gallego, C. Genotype-by-Environment Interactions for Seedling Establishment Across Native and Degraded-Forest Habitats in a Long-Lived Cycad. Bot. Rev. 79, 542–558 (2013). https://doi.org/10.1007/s12229-013-9124-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12229-013-9124-9