Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

Abstract One of the most intriguing questions in plant ecology is which evolutionary strategy allows widely distributed species to increase their ecological range and grow in changing environmental conditions. Phenotypic plasticity and local adaptations are major processes governing species range margins, but little is known about their relative contribution for tree species distribution in tropical forest regions. We investigated the relative role of phenotypic plasticity and local adaptation in the ecological distribution of the widespread palm Euterpe edulis in the Brazilian Atlantic Forest. Genetic sampling and experiments were performed in old‐growth remnants of two forest types with higher (Seasonal Semideciduous Forests vs. Submontane Rainforest) and lower biogeographic association and environmental similarities (Submontane Rainforest vs. Restinga Forest). We first assessed the molecular genetic differentiation among populations, focusing on the group of loci potentially under selection in each forest, using single‐nucleotide polymorphism (SNPs) outliers. Further, we looked for potential adaptive divergence among populations in a common garden experiment and in reciprocal transplants for two plant development phases: seedling establishment and sapling growth. Analysis with outlier loci indicated that all individuals from the Semideciduous Forest formed a single group, while another group was formed by overlapping individuals from Submontane Rainforest and Restinga Forest. Molecular differentiation was corroborated by reciprocal transplants, which yielded strong evidence of local adaptations for seedling establishment in the biogeographically divergent Rainforest and Semideciduous Forest, but not for Restinga Forest and Submontane Rainforest. Phenotypic plasticity for palm seedling establishment favors range expansion to biogeographically related or recently colonized forest types, while persistence in the newly colonized ecosystem may be favored by local adaptations if climatic conditions diverge over time, reducing gene flow between populations. SNPs obtained by next‐generation sequencing can help exploring adaptive genetic variation in tropical trees, which impose several challenges to the use of reciprocal transplants.

[1]  Anthony R. Ives,et al.  Temporal coexistence mechanisms contribute to the latitudinal gradient in forest diversity , 2017, Nature.

[2]  S. Bonser,et al.  Seedling response to environmental variability: The relationship between phenotypic plasticity and evolutionary history in closely related Eucalyptus species. , 2017, American journal of botany.

[3]  Craig Moritz,et al.  Exon capture phylogenomics: efficacy across scales of divergence , 2016, Molecular ecology resources.

[4]  C. Fraser,et al.  The importance of replicating genomic analyses to verify phylogenetic signal for recently evolved lineages , 2016, Molecular ecology.

[5]  Vít Latzel,et al.  Local adaptation of annual weed populations to habitats differing in disturbance regime , 2016, Evolutionary Ecology.

[6]  J. Ågren,et al.  Early life stages contribute strongly to local adaptation in Arabidopsis thaliana , 2016, Proceedings of the National Academy of Sciences.

[7]  R. Pennington,et al.  The contrasting nature of woody plant species in different neotropical forest biomes reflects differences in ecological stability. , 2016, The New phytologist.

[8]  Marcelino A. R. Pascoa,et al.  Establishment of tree seedlings in the understory of restoration plantations: natural regeneration and enrichment plantings , 2016 .

[9]  P. V. Eisenlohr,et al.  Revisiting Patterns of Tree Species Composition and their Driving Forces in the Atlantic Forests of Southeastern Brazil , 2015 .

[10]  Jason G. Bragg,et al.  Genomic variation across landscapes: insights and applications. , 2015, The New phytologist.

[11]  David Kenfack,et al.  An estimate of the number of tropical tree species , 2015, Proceedings of the National Academy of Sciences.

[12]  M. Ribeiro,et al.  Contemporary and historic factors influence differently genetic differentiation and diversity in a tropical palm , 2015, Heredity.

[13]  D. Schemske,et al.  Ecological differentiation and local adaptation in two sister species of Neotropical Costus (Costaceae). , 2015, Ecology.

[14]  P. Brancalion,et al.  When and how could common gardens be useful in the ecological restoration of long-lived tropical plants as an aid to the selection of seed sources? , 2015 .

[15]  A. Nicotra,et al.  The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. , 2014, Ecology letters.

[16]  J. Metzger,et al.  Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. , 2014, The New phytologist.

[17]  H. H. Bruun,et al.  An evaluation of seed zone delineation using phenotypic and population genomic data on black alder Alnus glutinosa , 2014 .

[18]  P. Brancalion,et al.  Can overharvesting of a non-timber-forest-product change the regeneration dynamics of a tropical rainforest? The case study of Euterpe edulis , 2014 .

[19]  S. Lavorel,et al.  The importance of biotic interactions and local adaptation for plant response to environmental changes: field evidence along an elevational gradient , 2014, Global change biology.

[20]  Zhian N. Kamvar,et al.  Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction , 2014, PeerJ.

[21]  S. Aitken,et al.  Evolutionary and plastic responses to climate change in terrestrial plant populations , 2013, Evolutionary applications.

[22]  Stephen P Hubbell,et al.  Tropical rain forest conservation and the twin challenges of diversity and rarity , 2013, Ecology and evolution.

[23]  Thomas F. Cross,et al.  diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors , 2013 .

[24]  Angel Amores,et al.  Stacks: an analysis tool set for population genomics , 2013, Molecular ecology.

[25]  P. Brancalion,et al.  Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size , 2013, Science.

[26]  Bettina M. J. Engelbrecht,et al.  Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees , 2013, Proceedings of the National Academy of Sciences.

[27]  Jonathan M. Chase,et al.  Beta-diversity in temperate and tropical forests reflects dissimilar mechanisms of community assembly. , 2013, Ecology letters.

[28]  H. Kroon,et al.  Root plasticity maintains growth of temperate grassland species under pulsed water supply , 2013, Plant and Soil.

[29]  Lindsay A. Turnbull,et al.  Identification of 100 fundamental ecological questions , 2013 .

[30]  P. Brancalion,et al.  Soil-mediated effects on potential Euterpe edulis (Arecaceae) fruit and palm heart sustainable management in the Brazilian Atlantic Forest , 2012 .

[31]  O. François,et al.  Adaptive Genetic Variation on the Landscape: Methods and Cases , 2012 .

[32]  F. Allendorf,et al.  Harnessing genomics for delineating conservation units. , 2012, Trends in ecology & evolution.

[33]  H. Hoekstra,et al.  Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species , 2012, PloS one.

[34]  J. Terborgh,et al.  Historical effects on beta diversity and community assembly in Amazonian trees , 2012, Proceedings of the National Academy of Sciences.

[35]  H. Balslev,et al.  Geographical ecology of the palms (Arecaceae): determinants of diversity and distributions across spatial scales. , 2011, Annals of botany.

[36]  H. Hoekstra,et al.  Molecular spandrels: tests of adaptation at the genetic level , 2011, Nature Reviews Genetics.

[37]  P. Brancalion,et al.  Seed development, yield and quality of two palm species growing in different tropical forest types in SE Brazil: implications for ecological restoration , 2011 .

[38]  C. Joly,et al.  Brazilian Atlantic Forest lato sensu: the most ancient Brazilian forest, and a biodiversity hotspot, is highly threatened by climate change. , 2010, Brazilian journal of biology = Revista brasleira de biologia.

[39]  G. Luikart,et al.  Genomics and the future of conservation genetics , 2010, Nature Reviews Genetics.

[40]  Keenan M. L. Mack,et al.  Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest , 2010, Nature.

[41]  Patrick J. McIntyre,et al.  Evolution and Ecology of Species Range Limits , 2009 .

[42]  Flávio J. M. Santos,et al.  Unusual branching in the palm Euterpe edulis Mart , 2009 .

[43]  Jean Paul Metzger,et al.  The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation , 2009 .

[44]  A. Zuur,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[45]  M. Heuertz,et al.  The Complex Biogeographic History of a Widespread Tropical Tree Species , 2008, Evolution; international journal of organic evolution.

[46]  Gordon Luikart,et al.  LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method , 2008, BMC Bioinformatics.

[47]  T. Jombart adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[48]  J. Ormerod,et al.  Extending the Linear Model With R: Generalized Linear, Mixed Effects and Nonparametric Regression Models , 2007, Statistics in Medicine.

[49]  H. Hoekstra,et al.  THE STUDY OF ADAPTATION AND SPECIATION IN THE GENOMIC ERA , 2007 .

[50]  C. C. Martins,et al.  Isoenzimas na diferenciação de sementes de três espécies do gênero Euterpe , 2007 .

[51]  M. Pigliucci,et al.  Phenotypic plasticity and evolution by genetic assimilation , 2006, Journal of Experimental Biology.

[52]  H. Balslev,et al.  Environmental and spatial controls of palm (Arecaceae) species richness across the Americas , 2005 .

[53]  Julie R. Etterson,et al.  EVOLUTIONARY RESPONSES TO CHANGING CLIMATE , 2005 .

[54]  J. F. Storz,et al.  INVITED REVIEW: Using genome scans of DNA polymorphism to infer adaptive population divergence , 2005, Molecular ecology.

[55]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[56]  M. Ashton,et al.  Soil‐related habitat specialization in dipterocarp rain forest tree species in Borneo , 2004 .

[57]  P. Coley,et al.  Herbivores Promote Habitat Specialization by Trees in Amazonian Forests , 2004, Science.

[58]  J. Faraway Extending the Linear Model with R , 2004 .

[59]  Jérôme Chave,et al.  Neutral theory and community ecology , 2004 .

[60]  D. Grattapaglia,et al.  Genetic structure, mating system, and long-distance gene flow in heart of palm (Euterpe edulis Mart.). , 2003, The Journal of heredity.

[61]  S. Mazer,et al.  Plant ecotypes: genetic differentiation in the age of ecological restoration , 2003 .

[62]  F. Scarano,et al.  Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. , 2002, Annals of botany.

[63]  J. Bever,et al.  LOCAL ADAPTATION IN THE LINUM MARGINALE—MELAMPSORA LINI HOST‐PATHOGEN INTERACTION , 2002, Evolution; international journal of organic evolution.

[64]  J. Pereira,et al.  How plants cope with water stress in the field. Photosynthesis and growth. , 2002, Annals of botany.

[65]  L. Morellato,et al.  Introduction: The Brazilian Atlantic Forest1 , 2000 .

[66]  Ary,et al.  Patterns of Floristic Differentiation among Atlantic Forests in Southeastern Brazil and the Influence of Climate 1 , 2000 .

[67]  Ary T. Oliveira-Filho,et al.  Patterns of Floristic Differentiation among Atlantic Forests in Southeastern Brazil and the Influence of Climate1 , 2000 .

[68]  J. Provan,et al.  Genetic differentiation of Euterpe edulis Mart. populations estimated by AFLP analysis , 2000, Molecular ecology.

[69]  C. Fenster,et al.  POPULATION DIFFERENTIATION IN AN ANNUAL LEGUME: GENETIC ARCHITECTURE , 2000, Evolution; international journal of organic evolution.

[70]  R. Mittermeier,et al.  Biodiversity hotspots for conservation priorities , 2000, Nature.

[71]  J. Svenning,et al.  Microhabitat specialization in a species‐rich palm community in Amazonian Ecuador , 1999 .

[72]  Fredrik Ronquist,et al.  Dispersal-Vicariance Analysis: A New Approach to the Quantification of Historical Biogeography , 1997 .

[73]  M. Beaumont,et al.  Evaluating loci for use in the genetic analysis of population structure , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  M. C. Grant,et al.  EVOLUTIONARY SIGNIFICANCE OF LOCAL GENETIC DIFFERENTIATION IN PLANTS , 1996 .

[75]  C. Schlichting,et al.  Phenotypic plasticity: an evolving plant character , 1986 .

[76]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[77]  A. Hendry Key Questions on the Role of Phenotypic Plasticity in Eco-Evolutionary Dynamics. , 2016, The Journal of heredity.

[78]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[79]  M. Swaine,et al.  Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic Forest , 2010, Biodiversity and Conservation.

[80]  T. Michael,et al.  METHODOLOGY ARTICLE Open Access , 2009 .

[81]  L. Alves,et al.  PALM SPECIES DISTRIBUTION AND SOIL MOISTURE IN A SWAMPY AREA OF THE ATLANTIC FOREST, SOUTH-EASTERN BRAZIL , 2008 .

[82]  Michdakis,et al.  A Generic Estimation of Population Subdivision Using Distances Between Alleles With Special Reference for Microsatellite Loci , 2002 .

[83]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .

[84]  Shivashankar H. Nagaraj,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .