Morphological plasticity and adaptation level of distylous Primula nivalis in a heterogeneous alpine environment
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摘要
Plant populations at high elevation face extreme climatic conditions and resource limitations. The existence of distylous species at different elevations can help us investigate their adaptation to high altitudes, the evolution of their morphological characteristics, as well as their responses to limited resources. Here, 17 populations of Primula nivalis at different elevations were evaluated regarding variations in plant morphological characteristics, biomass allocation, and morphological plasticity in a heterogeneous environment. Our results demonstrate that heterogeneous environments can affect plant morphological characteristics and resource allocation in each sexual morph of these plants. Moreover,environmental variations reduced morphological plasticity in the two plant morphs, and the plasticity of long style(LS) plants was greater than that of short style(SS) plants. There were significant negative correlations between morphological characteristics and elevation, rainfall, temperature, and sunshine,and these are the main variables that affect morphological characteristics and resource allocation of both morphs of P. nivalis plants in heterogeneous environments. The morphological characteristics of P. nivalis plants transplanted from high to lower elevations were not significantly different in either population.LS plants had greater morphological plasticity and adaptability in heterogeneous environments than SS plants. Elevational gradients and heterogeneous environments differentiated both morphs of P. nivalis plants with regards to morphology as well as adaptations. LS plants showed a higher level of adaptability than SS plants.
Plant populations at high elevation face extreme climatic conditions and resource limitations. The existence of distylous species at different elevations can help us investigate their adaptation to high altitudes, the evolution of their morphological characteristics, as well as their responses to limited resources. Here, 17 populations of Primula nivalis at different elevations were evaluated regarding variations in plant morphological characteristics, biomass allocation, and morphological plasticity in a heterogeneous environment. Our results demonstrate that heterogeneous environments can affect plant morphological characteristics and resource allocation in each sexual morph of these plants. Moreover,environmental variations reduced morphological plasticity in the two plant morphs, and the plasticity of long style(LS) plants was greater than that of short style(SS) plants. There were significant negative correlations between morphological characteristics and elevation, rainfall, temperature, and sunshine,and these are the main variables that affect morphological characteristics and resource allocation of both morphs of P. nivalis plants in heterogeneous environments. The morphological characteristics of P. nivalis plants transplanted from high to lower elevations were not significantly different in either population.LS plants had greater morphological plasticity and adaptability in heterogeneous environments than SS plants. Elevational gradients and heterogeneous environments differentiated both morphs of P. nivalis plants with regards to morphology as well as adaptations. LS plants showed a higher level of adaptability than SS plants.
Plant populations at high elevation face extreme climatic conditions and resource limitations. The existence of distylous species at different elevations can help us investigate their adaptation to high altitudes, the evolution of their morphological characteristics, as well as their responses to limited resources. Here, 17 populations of Primula nivalis at different elevations were evaluated regarding variations in plant morphological characteristics, biomass allocation, and morphological plasticity in a heterogeneous environment. Our results demonstrate that heterogeneous environments can affect plant morphological characteristics and resource allocation in each sexual morph of these plants. Moreover,environmental variations reduced morphological plasticity in the two plant morphs, and the plasticity of long style(LS) plants was greater than that of short style(SS) plants. There were significant negative correlations between morphological characteristics and elevation, rainfall, temperature, and sunshine,and these are the main variables that affect morphological characteristics and resource allocation of both morphs of P. nivalis plants in heterogeneous environments. The morphological characteristics of P. nivalis plants transplanted from high to lower elevations were not significantly different in either population.LS plants had greater morphological plasticity and adaptability in heterogeneous environments than SS plants. Elevational gradients and heterogeneous environments differentiated both morphs of P. nivalis plants with regards to morphology as well as adaptations. LS plants showed a higher level of adaptability than SS plants.
引文
Abdusalm,A.,2018. Effect of habitat heterogeneity on floral trait differentiation level in distylous species Primula nivalis. Acta.Bot. Boreal.-Occident.Sin.38,158-165.
Anderson,B.W.,Mccauley,S.,Lewis,G.P.,et al.,2014. Impacts of a Poultry processing plant on the diversity of escherichia coli populations and transferability of tetracycline resistance genes in an Urban Stream in South Carolina. Water Air Soil Poll 225,20-30.
Anderson,J.M.,Horton,P.,Kim,E.H.,et al.,2012. Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos Trans R Soc Lond B Biol Sci. 367,3515-3524.
Aragon,G.,Martinez,I.,Garcia,A.,2012. Loss of epiphytic diversity along a latitudinal gradient in southern Europe. Sci. Total Environ. 426,188-195.
Bradshaw,W.E.,Holzapfel,C.M.,2006. Evolutionary response to rapid climate change. Science 312,1477-1478.
Ceplick,G.P.,1995. Genotypic variation and plasticity of clonal growth in relation to nutrient availability in Amphibromus scabrivalvis. J. Ecol 83,459-468.
Dorken,M.E.,Barrett,S.C.H.,2004. Phenotypic plasticity of vegetative and reproductive traits Blackwell Publishing,Ltd. in monoecious and dioecious populations of Sagittaria latifolia(Alismataceae):a clonal aquatic plant. J. Ecol. 92,32-44.
Dudley,S.A.,Schmitt,J.,1996. Testing the adaptive plasticity hypothesis:densitydependent selection on manipulated stem length in Impatiens capensis. Am.Nat 147,445-465.
Frei,E.R.,Ghazoul,J.,Pluess,A.R.,2014. Plastic responses to elevated temperature in low and high elevation populations of three grassland species. PloS One 9(6),e98677. https://doi.org/10.1371/journal.pone.0098677.
Fusco,G.,Minelli,A.,2010. Phenotypic plasticity in development and evolution:facts and concepts. Philos. T. R. Soc. 365,547-556.
Godoy,O.,Saldana,A.,Fuentes,N.,et al.,2011. Forests are not immune to plant invasions:phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biol. Invasions 13,1615-1625.
Gianoli,E.,Valladares,F.,2010. Global change and the evolution of phenotypic plasticity in plants. Ann. NY. Acad. Sci. 1206,35-55.
Goh,C.H.,Vallejos,D.F.V.,Nicotra,A.B.,et al.,2013. The impact of beneficial plantassociated microbes on plant phenotypic plasticity. J. Chem. Ecol. 39,826-839.
Guerin,G.R.,Wen,H.X.,Lowe,A.J.,2012. Leaf morphology shifts linked to climate change. Biol. Lett. 8,882-886.
Gugger,S.,Kesselring,H.,Stocklin,J.,et al.,2015. Lower plasticity exhibited by highversus mid-elevation species in their phenological responses to manipulated temperature and drought. Ann. Bot. Lond. 116,953-962.
Gomez-Aparicio,L.,Zamora,R.,Gomez,J.M.,2005. The regeneration status of the endangered Acer opalus,subsp. granatense,throughout its geographical distribution in the Iberian Peninsula. Biol.Conserv. 121,195-206.
Herrera,C.M.,Bazaga,P.,2013. Epigenetic correlates of plant phenotypic plasticity:DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium(Aquifoliaceae)trees. Bot. J. Linn. Soc. 171,441-452.
Huber,H.,Jacobs,E.,Visser,E.J.W.,2009. Variation in flooding-induced morphological traits in natural populations of white clover(Trifolium repens)and their effects on plant performance during soil flooding. Ann. Bot. London. 103,377-386.
Hudson,J.M.C.,Henry,G.H.R.,Cornwell,W.K.,2011. Taller and larger:shifts in Arctic tundra leaf traits after 16 years of experimental warming. Global Change Biol.17,1013-1021.
Leingartner,A.,Hoiss,B.,Krauss,J.,et al.,2014. Combined effects of extreme climatic events and elevation on nutritional quality and herbivory of alpine plants. PloS one 9(4),e93881.
Lenoir,J.,Svenning,J.C.,2013. Latitudinal and elevational range shifts under contemporary climatecchange. Encyclopedia Biodiver 599-611.
Matesanz,S.,Gianoli,E.,Valladares,F.,2010. Global change and the evolution of phenotypic plasticity in plants. Ann. N.Y. Acad. Sci. 1206,35-55.
Miner,B.G.,Sultan,S.E.,Morgan,S.G.,et al.,2005. Ecological consequences of phenotypic plasticity. Trends. Ecol. Evol. 20,685-692.
Millal,R.,Reich,P.B.,2011. Multi-trait interactions,not phylogeny,fine-tune leaf size reduction with increasing altitude. Ann. Bot. Lond. 107,455-465.
Mou,P.,Jones,R.H.,Tan,Z.Q.,et al.,2013. Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous.Plant Soil 364,373-384.
Navas,M.L,Richard,J.M.,2005. Can traits predict the competitive response of herbaceous Mediterranean species? Acta Oecol 27,107-114.
Nascimbene,J.,Marini,L.,2015. Epiphytic lichen diversity along elevational gradients:biological traits reveal a complex response to water and energy.J. Biogeogr. 42,1222-1232.
Nicotra,A.B.,Atkin,O.K.,Bonser,S.P.,et al.,2010. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15,684-692.
Pizarro,LC.,Bisigato,A.J.,2010. Allocation of biomass and photoassimilates in juvenile plants of six Patagonian species in response to five water supply regimes.Ann. Bot. Lond. 106,297-307.
Puijalon,S.,Bornette,G.,2006. Phenotypic plasticity and mechanical stress:biomass partitioning and clonal growth of an aquatic plant species. Am. J. Bot.93,1090-1099.
Ramirez-Valiente,J.A.,Valladares,F.,Delgado,A.,et al.,2015. Understanding the importance of intrapopulation functional variability and phenotypic plasticity in Quercus suber. Tree Genet. Genomes 11,35.
Richards,C.L.,Bossdorf,0.,Muth,N.Z.,et al.,2006. Jack of all trades,master of some? On the role of phenotypic plasticity in plant invasions. Ecol. Lett. 9,981-993.
Scheiner,S.M.,2013. The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity. Ecol. Evol. 3,4596-4609.
Shen,H.H.,Tang,Y.H.,Muraoka,H.,et al.,2008. Characteristics of leaf photosynthesis and simulated individual carbon budget in Primula nutans under contrasting light and temperature conditions. J. Plant Res. 121,191-200.
Shimizu,K.K.,Kudoh,H.,Kobayashi,M.J.,2011. Plant sexual reproduction during climate change:gene function in nature studied by ecological and evolutionary systems biology. Ann. Bot. Lond. 108,777-787.
Tetard-Jones,C.,Kertesz,M.A.,Phil,R.F.P.,2011. Quantitative trait loci mapping of phenotypic plasticity and genotype-environment interactions in plant and insect performance. Philos. Trans. R. Soc. B 366,1368-1379.
Valladares,F.,Balaguer,L.,Martinez-Ferri,E.,2002. Plasticity,instability and canalization:Is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytol 156,457-467.
Valladares,F.,Matesanz,S.,Guilhaumon,F.,et al.,2014. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17,1351-1364.
Valladares,F.,Gianoli,E.,Gomez,J.M.,2007. Ecological limits to plant phenotypic plasticity. New Phytol. 176,749-763.
Wang,R.,Yu,G.,He,N.,et al.,2014. Elevation-related variation in leaf stomatal traits as a function of plant functional type:evidence from Changbai Mountain,China.PloS One 9(12),e115395. https://doi.org/10.1371/journal.pone.0115395.
Wu,R.,Grissom,J.E.,McKeand,S.E.,et al.,2004. Phenotypic plasticity of fine root growth increases plant productivity in pine seedlings. BMC Ecol. 4,14. https://doi.org/10.1186/1472-6785-4-14.
Xie,Y.H.,Luo,W.B.,Ren,B.,et al.,2007. Morphological and physiological responses to sediment type and light availability in roots of the submerged plant Myriophyllum spicatum. Ann. Bot. Lond. 100,1517-1523.
Zhang,X.,Izaurralde,R.C.,Arnold,J.G.,et al.,2011. Comment on"modeling miscanthus in the soil and water assessment tool(SWAT)to Simulate Its water quality effects as a bioenergy crop". Environ. Sci.Technol 45,6211-6212.
Anderson,B.W.,Mccauley,S.,Lewis,G.P.,et al.,2014. Impacts of a Poultry processing plant on the diversity of escherichia coli populations and transferability of tetracycline resistance genes in an Urban Stream in South Carolina. Water Air Soil Poll 225,20-30.
Anderson,J.M.,Horton,P.,Kim,E.H.,et al.,2012. Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos Trans R Soc Lond B Biol Sci. 367,3515-3524.
Aragon,G.,Martinez,I.,Garcia,A.,2012. Loss of epiphytic diversity along a latitudinal gradient in southern Europe. Sci. Total Environ. 426,188-195.
Bradshaw,W.E.,Holzapfel,C.M.,2006. Evolutionary response to rapid climate change. Science 312,1477-1478.
Ceplick,G.P.,1995. Genotypic variation and plasticity of clonal growth in relation to nutrient availability in Amphibromus scabrivalvis. J. Ecol 83,459-468.
Dorken,M.E.,Barrett,S.C.H.,2004. Phenotypic plasticity of vegetative and reproductive traits Blackwell Publishing,Ltd. in monoecious and dioecious populations of Sagittaria latifolia(Alismataceae):a clonal aquatic plant. J. Ecol. 92,32-44.
Dudley,S.A.,Schmitt,J.,1996. Testing the adaptive plasticity hypothesis:densitydependent selection on manipulated stem length in Impatiens capensis. Am.Nat 147,445-465.
Frei,E.R.,Ghazoul,J.,Pluess,A.R.,2014. Plastic responses to elevated temperature in low and high elevation populations of three grassland species. PloS One 9(6),e98677. https://doi.org/10.1371/journal.pone.0098677.
Fusco,G.,Minelli,A.,2010. Phenotypic plasticity in development and evolution:facts and concepts. Philos. T. R. Soc. 365,547-556.
Godoy,O.,Saldana,A.,Fuentes,N.,et al.,2011. Forests are not immune to plant invasions:phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biol. Invasions 13,1615-1625.
Gianoli,E.,Valladares,F.,2010. Global change and the evolution of phenotypic plasticity in plants. Ann. NY. Acad. Sci. 1206,35-55.
Goh,C.H.,Vallejos,D.F.V.,Nicotra,A.B.,et al.,2013. The impact of beneficial plantassociated microbes on plant phenotypic plasticity. J. Chem. Ecol. 39,826-839.
Guerin,G.R.,Wen,H.X.,Lowe,A.J.,2012. Leaf morphology shifts linked to climate change. Biol. Lett. 8,882-886.
Gugger,S.,Kesselring,H.,Stocklin,J.,et al.,2015. Lower plasticity exhibited by highversus mid-elevation species in their phenological responses to manipulated temperature and drought. Ann. Bot. Lond. 116,953-962.
Gomez-Aparicio,L.,Zamora,R.,Gomez,J.M.,2005. The regeneration status of the endangered Acer opalus,subsp. granatense,throughout its geographical distribution in the Iberian Peninsula. Biol.Conserv. 121,195-206.
Herrera,C.M.,Bazaga,P.,2013. Epigenetic correlates of plant phenotypic plasticity:DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium(Aquifoliaceae)trees. Bot. J. Linn. Soc. 171,441-452.
Huber,H.,Jacobs,E.,Visser,E.J.W.,2009. Variation in flooding-induced morphological traits in natural populations of white clover(Trifolium repens)and their effects on plant performance during soil flooding. Ann. Bot. London. 103,377-386.
Hudson,J.M.C.,Henry,G.H.R.,Cornwell,W.K.,2011. Taller and larger:shifts in Arctic tundra leaf traits after 16 years of experimental warming. Global Change Biol.17,1013-1021.
Leingartner,A.,Hoiss,B.,Krauss,J.,et al.,2014. Combined effects of extreme climatic events and elevation on nutritional quality and herbivory of alpine plants. PloS one 9(4),e93881.
Lenoir,J.,Svenning,J.C.,2013. Latitudinal and elevational range shifts under contemporary climatecchange. Encyclopedia Biodiver 599-611.
Matesanz,S.,Gianoli,E.,Valladares,F.,2010. Global change and the evolution of phenotypic plasticity in plants. Ann. N.Y. Acad. Sci. 1206,35-55.
Miner,B.G.,Sultan,S.E.,Morgan,S.G.,et al.,2005. Ecological consequences of phenotypic plasticity. Trends. Ecol. Evol. 20,685-692.
Millal,R.,Reich,P.B.,2011. Multi-trait interactions,not phylogeny,fine-tune leaf size reduction with increasing altitude. Ann. Bot. Lond. 107,455-465.
Mou,P.,Jones,R.H.,Tan,Z.Q.,et al.,2013. Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous.Plant Soil 364,373-384.
Navas,M.L,Richard,J.M.,2005. Can traits predict the competitive response of herbaceous Mediterranean species? Acta Oecol 27,107-114.
Nascimbene,J.,Marini,L.,2015. Epiphytic lichen diversity along elevational gradients:biological traits reveal a complex response to water and energy.J. Biogeogr. 42,1222-1232.
Nicotra,A.B.,Atkin,O.K.,Bonser,S.P.,et al.,2010. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15,684-692.
Pizarro,LC.,Bisigato,A.J.,2010. Allocation of biomass and photoassimilates in juvenile plants of six Patagonian species in response to five water supply regimes.Ann. Bot. Lond. 106,297-307.
Puijalon,S.,Bornette,G.,2006. Phenotypic plasticity and mechanical stress:biomass partitioning and clonal growth of an aquatic plant species. Am. J. Bot.93,1090-1099.
Ramirez-Valiente,J.A.,Valladares,F.,Delgado,A.,et al.,2015. Understanding the importance of intrapopulation functional variability and phenotypic plasticity in Quercus suber. Tree Genet. Genomes 11,35.
Richards,C.L.,Bossdorf,0.,Muth,N.Z.,et al.,2006. Jack of all trades,master of some? On the role of phenotypic plasticity in plant invasions. Ecol. Lett. 9,981-993.
Scheiner,S.M.,2013. The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity. Ecol. Evol. 3,4596-4609.
Shen,H.H.,Tang,Y.H.,Muraoka,H.,et al.,2008. Characteristics of leaf photosynthesis and simulated individual carbon budget in Primula nutans under contrasting light and temperature conditions. J. Plant Res. 121,191-200.
Shimizu,K.K.,Kudoh,H.,Kobayashi,M.J.,2011. Plant sexual reproduction during climate change:gene function in nature studied by ecological and evolutionary systems biology. Ann. Bot. Lond. 108,777-787.
Tetard-Jones,C.,Kertesz,M.A.,Phil,R.F.P.,2011. Quantitative trait loci mapping of phenotypic plasticity and genotype-environment interactions in plant and insect performance. Philos. Trans. R. Soc. B 366,1368-1379.
Valladares,F.,Balaguer,L.,Martinez-Ferri,E.,2002. Plasticity,instability and canalization:Is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytol 156,457-467.
Valladares,F.,Matesanz,S.,Guilhaumon,F.,et al.,2014. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17,1351-1364.
Valladares,F.,Gianoli,E.,Gomez,J.M.,2007. Ecological limits to plant phenotypic plasticity. New Phytol. 176,749-763.
Wang,R.,Yu,G.,He,N.,et al.,2014. Elevation-related variation in leaf stomatal traits as a function of plant functional type:evidence from Changbai Mountain,China.PloS One 9(12),e115395. https://doi.org/10.1371/journal.pone.0115395.
Wu,R.,Grissom,J.E.,McKeand,S.E.,et al.,2004. Phenotypic plasticity of fine root growth increases plant productivity in pine seedlings. BMC Ecol. 4,14. https://doi.org/10.1186/1472-6785-4-14.
Xie,Y.H.,Luo,W.B.,Ren,B.,et al.,2007. Morphological and physiological responses to sediment type and light availability in roots of the submerged plant Myriophyllum spicatum. Ann. Bot. Lond. 100,1517-1523.
Zhang,X.,Izaurralde,R.C.,Arnold,J.G.,et al.,2011. Comment on"modeling miscanthus in the soil and water assessment tool(SWAT)to Simulate Its water quality effects as a bioenergy crop". Environ. Sci.Technol 45,6211-6212.