Fast–slow continuum and reproductive strategies structure plant life-history variation worldwide

Significance Schedules of survival, growth, and reproduction define life-history strategies across species. Understanding how life-history strategies are structured is fundamental to our understanding of the evolution, abundance, and distribution of species. We found that life-history strategies of 418 plant species worldwide are explained by an axis representing the pace of life and another representing the wide range of reproductive strategies. This framework predicts responses to perturbations and long-term population performance, showing great promise as a predictive tool for plant population responses to environmental change. The identification of patterns in life-history strategies across the tree of life is essential to our prediction of population persistence, extinction, and diversification. Plants exhibit a wide range of patterns of longevity, growth, and reproduction, but the general determinants of this enormous variation in life history are poorly understood. We use demographic data from 418 plant species in the wild, from annual herbs to supercentennial trees, to examine how growth form, habitat, and phylogenetic relationships structure plant life histories and to develop a framework to predict population performance. We show that 55% of the variation in plant life-history strategies is adequately characterized using two independent axes: the fast–slow continuum, including fast-growing, short-lived plant species at one end and slow-growing, long-lived species at the other, and a reproductive strategy axis, with highly reproductive, iteroparous species at one extreme and poorly reproductive, semelparous plants with frequent shrinkage at the other. Our findings remain consistent across major habitats and are minimally affected by plant growth form and phylogenetic ancestry, suggesting that the relative independence of the fast–slow and reproduction strategy axes is general in the plant kingdom. Our findings have similarities with how life-history strategies are structured in mammals, birds, and reptiles. The position of plant species populations in the 2D space produced by both axes predicts their rate of recovery from disturbances and population growth rate. This life-history framework may complement trait-based frameworks on leaf and wood economics; together these frameworks may allow prediction of responses of plants to anthropogenic disturbances and changing environments.

[1]  Ming Dong,et al.  The compadre Plant Matrix Database: an open online repository for plant demography , 2015 .

[2]  N. Besansky Malaria: How vector mosquitoes beat the heat , 2014, Nature.

[3]  J. Gaillard,et al.  Influence of Life-History Tactics on Transient Dynamics: A Comparative Analysis across Mammalian Populations , 2014, The American Naturalist.

[4]  A. Yoder,et al.  Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species , 2014, BMC Evolutionary Biology.

[5]  Peter B. Adler,et al.  Functional traits explain variation in plant life history strategies , 2013, Proceedings of the National Academy of Sciences.

[6]  J. S. Boatwright,et al.  Advances in legume systematics 12 , 2013 .

[7]  Jerrold I. Davis,et al.  Phylogeny of the Liliales (Monocotyledons) with special emphasis on data partition congruence and RNA editing , 2013, Cladistics : the international journal of the Willi Hennig Society.

[8]  K. Yeh,et al.  Small RNAs of Sequoia sempervirens during rejuvenation and phase change. , 2013, Plant biology.

[9]  A. Vovides,et al.  A modification to the SCAR (Sequence Characterized Amplified Region) method provides phylogenetic insights within Ceratozamia (Zamiaceae) , 2015 .

[10]  L. Harmon,et al.  OneZoom: A Fractal Explorer for the Tree of Life , 2012, PLoS biology.

[11]  L. Hufford,et al.  A Broad Phylogenetic Analysis of Boraginaceae: Implications for the Relationships of Mertensia , 2012 .

[12]  Scott Federhen,et al.  The NCBI Taxonomy database , 2011, Nucleic Acids Res..

[13]  D. Khasa,et al.  Phylogeny, diversification rates and species boundaries of Mesoamerican firs (Abies, Pinaceae) in a genus-wide context. , 2012, Molecular phylogenetics and evolution.

[14]  G. Salazar,et al.  Molecular phylogeny of Cypripedium (Orchidaceae: Cypripedioideae) inferred from multiple nuclear and chloroplast regions. , 2011, Molecular phylogenetics and evolution.

[15]  S. Higgins,et al.  TRY – a global database of plant traits , 2011, Global Change Biology.

[16]  D. Soltis,et al.  Multi-gene analysis provides a well-supported phylogeny of Rosales. , 2011, Molecular phylogenetics and evolution.

[17]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[18]  Dale M Edgar,et al.  Hibernation in Black Bears: Independence of Metabolic Suppression from Body Temperature , 2011, Science.

[19]  T. Hodkinson,et al.  Phylogenetics of Panicoideae (Poaceae) based on chloroplast and nuclear DNA sequences , 2011 .

[20]  R. Salguero‐Gómez,et al.  A hydraulic explanation for size-specific plant shrinkage: developmental hydraulic sectoriality. , 2011, The New phytologist.

[21]  Elizabeth E Crone,et al.  How do plant ecologists use matrix population models? , 2011, Ecology letters.

[22]  M. Chase,et al.  Molecular phylogenetics of Ruscaceae sensu lato and related families (Asparagales) based on plastid and nuclear DNA sequences. , 2010, Annals of botany.

[23]  Roberto Salguero-Gómez,et al.  Matrix Dimensions Bias Demographic Inferences: Implications for Comparative Plant Demography , 2010, The American Naturalist.

[24]  William F. Morris,et al.  Demographic compensation and tipping points in climate-induced range shifts , 2010, Nature.

[25]  N. Alvarez,et al.  Phylogeny and circumscription of Sapindaceae revisited: molecular sequence data, morphology and biogeography support recognition of a new family, Xanthoceraceae. , 2010 .

[26]  J. Peñuelas,et al.  Potentially immortal? , 2010, The New phytologist.

[27]  P. Lockhart,et al.  A molecular phylogeny, morphology and classification of genera of Ranunculeae (Ranunculaceae) , 2010 .

[28]  P. Peterson,et al.  A classification of the Chloridoideae (Poaceae) based on multi-gene phylogenetic trees. , 2010, Molecular phylogenetics and evolution.

[29]  S. Townley,et al.  Boom or bust? A comparative analysis of transient population dynamics in plants , 2010 .

[30]  R. Salguero‐Gómez,et al.  Keeping plant shrinkage in the demographic loop , 2010 .

[31]  P. Bah Toward a phylogenetic subfamilial classification for the Compositae (Asteraceae) , 2010 .

[32]  Liam J. Revell,et al.  Size-Correction and Principal Components for Interspecific Comparative Studies , 2009, Evolution; international journal of organic evolution.

[33]  Yongfang Xie,et al.  Molecular phylogeny of Ranunculaceae based on internal transcribed spacer sequences , 2009 .

[34]  K. Kron,et al.  A Large‐Scale Phylogeny of Polygonaceae Based on Molecular Data , 2009, International Journal of Plant Sciences.

[35]  M. Chase,et al.  A subfamilial classification for the expanded asparagalean families Amaryllidaceae, Asparagaceae and Xanthorrhoeaceae , 2009 .

[36]  Richard P. Shefferson The evolutionary ecology of vegetative dormancy in mature herbaceous perennial plants , 2009 .

[37]  Shawn W. Laffan,et al.  Global patterns in plant height , 2009 .

[38]  A. S. Alvarado Developmental biology: A cellular view of regeneration , 2009, Nature.

[39]  B. Bremer,et al.  Time Tree of Rubiaceae: Phylogeny and Dating the Family, Subfamilies, and Tribes , 2009, International Journal of Plant Sciences.

[40]  H. Schenk,et al.  Hydraulically integrated or modular? Comparing whole-plant-level hydraulic systems between two desert shrub species with different growth forms. , 2009, The New phytologist.

[41]  P. Vargas,et al.  Historical biogeography and character evolution of Cistaceae (Malvales) based on analysis of plastid rbcL and trnL-trnF sequences , 2009 .

[42]  Geoffrey B. West,et al.  A general quantitative theory of forest structure and dynamics , 2009, Proceedings of the National Academy of Sciences.

[43]  J. Chave,et al.  Towards a Worldwide Wood Economics Spectrum 2 . L E a D I N G D I M E N S I O N S I N W O O D F U N C T I O N , 2022 .

[44]  K. Matsuura,et al.  Queen Succession Through Asexual Reproduction in Termites , 2009, Science.

[45]  Zhiduan Chen,et al.  Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data , 2009 .

[46]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[47]  V. Funk,et al.  Compositae Metatrees: The Next Generation , 2009 .

[48]  Alejandro Sánchez Alvarado Developmental biology: A cellular view of regeneration. , 2009, Nature.

[49]  V. Funk,et al.  Classification of Compositae , 2009 .

[50]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[51]  M. Chase,et al.  Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. , 2008, Molecular phylogenetics and evolution.

[52]  D. Gónzalez,et al.  Phylogenetic Relationships of the Neotropical Genus Dioon (Cycadales, Zamiaceae) Based on Nuclear and Chloroplast DNA Sequence Data , 2008 .

[53]  H. de Kroon,et al.  Demographic vulnerability of the clonal and endangered meadow thistle , 2008, Plant Ecology.

[54]  P. Stevens,et al.  Phylogenetic classification of Ericaceae: Molecular and morphological evidence , 2002, The Botanical Review.

[55]  Sandra M. Brasfield,et al.  Reproductive and thyroid hormone profiles in captive Western fence lizards (Sceloporus occidentalis) after a period of brumation. , 2008, Zoo biology.

[56]  B. Kendall,et al.  Longevity can buffer plant and animal populations against changing climatic variability. , 2008, Ecology.

[57]  C. Kyriacou,et al.  A Molecular Basis for Natural Selection at the timeless Locus in Drosophila melanogaster , 2007, Science.

[58]  D. R. Morgan,et al.  Phylogeny and classification of Rosaceae , 2007, Plant Systematics and Evolution.

[59]  J. L. Gittleman,et al.  The Fast‐Slow Continuum in Mammalian Life History: An Empirical Reevaluation , 2007, The American Naturalist.

[60]  C Jessica E Metcalf,et al.  Why evolutionary biologists should be demographers. , 2007, Trends in ecology & evolution.

[61]  P. Weston,et al.  A new suprageneric classification of the Proteaceae, with an annotated checklist of genera , 2006 .

[62]  Charles James Nice Bailey,et al.  Toward a global phylogeny of the Brassicaceae. , 2006, Molecular biology and evolution.

[63]  B. Hall,et al.  Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses. , 2006, Molecular phylogenetics and evolution.

[64]  E. Kellogg,et al.  Brassicaceae phylogeny and trichome evolution. , 2006, American journal of botany.

[65]  L. Minuto,et al.  Molecular phylogeny of the Caryophyllaceae (Caryophyllales) inferred from chloroplast matK and nuclear rDNA ITS sequences. , 2006, American journal of botany.

[66]  P. D. Tredici Aging and Rejuvenation in Trees , 2006 .

[67]  Heather North,et al.  Slowing down a pine invasion despite uncertainty in demography and dispersal , 2005 .

[68]  T. J. Edwards Advances in Legume Systematics, Part 10: Higher Level Systematics , 2005 .

[69]  S. Chaw,et al.  A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region. , 2005, Molecular phylogenetics and evolution.

[70]  Jean-Michel Gaillard,et al.  Generation Time: A Reliable Metric to Measure Life‐History Variation among Mammalian Populations , 2005, The American Naturalist.

[71]  Campbell O. Webb,et al.  Phylomatic: tree assembly for applied phylogenetics , 2005 .

[72]  A. Liston,et al.  Phylogeny and classification of Pinus , 2005 .

[73]  Bengt Oxelman,et al.  Piecing together the "new" Plantaginaceae. , 2005, American journal of botany.

[74]  T. Stuessy,et al.  Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions. , 2005, American journal of botany.

[75]  Madan K. Oli,et al.  The fast–slow continuum and mammalian life-history patterns: an empirical evaluation , 2004 .

[76]  Jens-Christian Svenning,et al.  ECOLOGICAL DETERMINISM IN PLANT COMMUNITY STRUCTURE ACROSS A TROPICAL FOREST LANDSCAPE , 2004 .

[77]  M. Neubert,et al.  Projecting Rates of Spread for Invasive Species , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[78]  M. Westoby,et al.  Seedling survival and seed size: a synthesis of the literature , 2004 .

[79]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[80]  M. Chase,et al.  An expanded plastid DNA phylogeny of Orchidaceae and analysis of jackknife branch support strategy. , 2004, American journal of botany.

[81]  D. Doak,et al.  Book Review: Quantitative Conservation biology: Theory and Practice of Population Viability analysis , 2004, Landscape Ecology.

[82]  Robert K Jansen,et al.  ITS secondary structure derived from comparative analysis: implications for sequence alignment and phylogeny of the Asteraceae. , 2003, Molecular phylogenetics and evolution.

[83]  R. Price GENERIC AND FAMILIAL RELATIONSHIPS OF THE TAXACEAE FROM RBCL AND MATK SEQUENCE COMPARISONS , 2003 .

[84]  John Sabo,et al.  Morris, W. F., and D. F. Doak. 2003. Quantitative Conservation Biology: Theory and Practice of Population Viability Analysis. Sinauer Associates, Sunderland, Massachusetts, USA , 2003 .

[85]  M. Chase,et al.  Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences. , 2003, American journal of botany.

[86]  R. Jansen,et al.  Phylogeny of Campanulaceae S. Str. Inferred from Its Sequences of Nuclear Ribosomal DNA , 2003 .

[87]  M. Pagel,et al.  Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence , 2002, The American Naturalist.

[88]  Jocelyn C Hall,et al.  Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. , 2002, American journal of botany.

[89]  Michael D. Collins,et al.  The unified neutral theory of biodiversity and biogeography , 2002 .

[90]  Mark W. Chase,et al.  Evolution of the angiosperms: calibrating the family tree , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[91]  Charles H. Cannon,et al.  Systematics of Fagaceae: Phylogenetic Tests of Reproductive Trait Evolution , 2001, International Journal of Plant Sciences.

[92]  E. Kellogg,et al.  A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. , 2001, American journal of botany.

[93]  G. Powell,et al.  Terrestrial Ecoregions of the World: A New Map of Life on Earth , 2001 .

[94]  K. Bremer,et al.  Age and biogeography of major clades in Liliales. , 2001, American journal of botany.

[95]  A. Chanderbali,et al.  Phylogeny and Historical Biogeography of Lauraceae: Evidence from the Chloroplast and Nuclear Genomes , 2001 .

[96]  Jerrold I. Davis,et al.  Phylogeny and subfamilial classification of the grasses (Poaceae) , 2001 .

[97]  H. Caswell Matrix population models : construction, analysis, and interpretation , 2001 .

[98]  M. Donoghue,et al.  phylogeny and phylogenetic taxonomy of dipsacales, with special reference to sinadoxa and tetradoxa (adoxaceae) , 2001 .

[99]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[100]  M. Simpson,et al.  Phylogenetic Relationships in the Commelinaceae: I. A Cladistic Analysis of Morphological Data , 2000 .

[101]  Polemoniaceae phylogeny and classification: implications of sequence data from the chloroplast gene ndhF. , 2000, American journal of botany.

[102]  P. Gadek,et al.  Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach. , 2000, American journal of botany.

[103]  J. Palmer,et al.  Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[104]  W. Zhang,et al.  Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data. , 2000, Molecular phylogenetics and evolution.

[105]  Victor A. Albert,et al.  A phylogenetic analysis of the Orchidaceae: evidence from rbcL nucleotide. , 1999, American journal of botany.

[106]  C. Baskin,et al.  Seeds: Ecology, Biogeography, and, Evolution of Dormancy and Germination , 1998 .

[107]  R. Olmstead,et al.  Examination of subfamilial phylogeny in Bromeliaceae using comparative sequencing of the plastid locus ndhF. , 1997, American journal of botany.

[108]  R. Díaz-Uriarte,et al.  Covariation of Life-History Traits in Lacertid Lizards: A Comparative Study , 1997, The American Naturalist.

[109]  A. Zharkikh,et al.  Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences. , 1997, Molecular biology and evolution.

[110]  J. Silvertown,et al.  Life history variation in plants: an exploration of the fast-slow continuum hypothesis , 1996 .

[111]  Eric S. Menges,et al.  Interpretation of elasticity matrices as an aid to the management of plant populations for conservation , 1996 .

[112]  T. Hughes,et al.  Reproductive Strategies of Modular Organisms: Comparative Studies of Reef‐ Building Corals , 1996 .

[113]  J. Silvertown,et al.  On Trade-Offs, Elasticities and the Comparative Method: A Reply to Shea, Rees & Wood , 1994 .

[114]  K. Shea,et al.  Trade-Offs, elasticities and the comparative method , 1994 .

[115]  M. Rees Trade-offs among dispersal strategies in British plants , 1993, Nature.

[116]  M. Donoghue,et al.  Phylogenetic relationships of Dipsacales based on rbcl sequences , 1992 .

[117]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[118]  M. Franco Plant demography : What do we know? , 1990 .

[119]  J. Gaillard,et al.  An analysis of demographic tactics in birds and mammals , 1989 .

[120]  T. R. E. Southwood,et al.  Tactics, strategies and templets* , 1988 .

[121]  B. Sæther The Influence of Body Weight on the Covariation between Reproductive Traits in European Birds , 1987 .

[122]  Jacqueline K. White,et al.  Some Life-History Consequences of Modular Construction in Plants , 1986 .

[123]  A. Dunham,et al.  Patterns of Covariation in Life History Traits of Squamate Reptiles: The Effects of Size and Phylogeny Reconsidered , 1985, The American Naturalist.

[124]  S. Stearns The influence of size and phylogeny on patterns of covariation among life-history traits in the mammals , 1983 .

[125]  R. Lande,et al.  A Quantitative Genetic Theory of Life History Evolution , 1982 .

[126]  Paulette Bierzychudek,et al.  The Demography of Jack‐in‐the‐Pulpit, a Forest Perennial that Changes Sex , 1982 .

[127]  D. Western Size, life history and ecology in mammals , 1979 .

[128]  J. Harper,et al.  The Demography of Plants , 1974 .

[129]  C. Raunkiær,et al.  The life forms of plants and statistical plant geography , 1934 .

[130]  A. Backlund Phylogeny of the Asteridae s . str . based on rbcL sequences , with particular reference to the Dipsacales , 2022 .