1932

Abstract

Flowering plants exhibit two principal life-history strategies: annuality (living and reproducing in one year) and perenniality (living more than one year). The advantages of either strategy depend on the relative benefits of immediate reproduction balanced against survivorship and future reproduction. This trade-off means that life-history strategies are associated with particular environments, with annuals being found more often in unpredictable habitats. Annuality and perenniality are the outcome of developmental genetic programs responding to their environment, with perennials being distinguished by their delayed competence to flower and reversion to growth after flowering. Evolutionary transitions between these strategies are frequent and have consequences for mating systems and genome evolution, with perennials being more likely to outcross with higher inbreeding depression and lower rates of molecular evolution. Integrating expectations from life-history theory with knowledge of the developmental genetics of flowering and seasonality is required to understand the mechanisms involved in the evolution of annual and perennial life histories.

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2020-11-02
2024-05-24
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Literature Cited

  1. Aikawa S, Kobayashi MJ, Satake A, Shimizu KK, Kudoh H 2010. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. PNAS 107:2511632–37
    [Google Scholar]
  2. Albani MC, Coupland G. 2010. Comparative analysis of flowering in annual and perennial plants. Plant Development MCP Timmermans 323–48 Curr. Top. Dev. Biol 91 Amsterdam: Elsevier
    [Google Scholar]
  3. Amasino RM. 2010. Seasonal and developmental timing of flowering. Plant J 61:61001–13
    [Google Scholar]
  4. Andreasen K, Baldwin BG. 2001. Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S-26S rDNA internal and external transcribed spacers. Mol. Biol. Evol. 18:6936–44
    [Google Scholar]
  5. Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13:9627–39
    [Google Scholar]
  6. Angeloni F, Ouborg NJ, Leimu R 2011. Meta‐analysis on the association of population size and life history with inbreeding depression in plants. Biol. Conserv. 144:35–43
    [Google Scholar]
  7. Angiosperm Phylogeny Group. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181:11–20
    [Google Scholar]
  8. Archibald JK, Mort ME, Crawford DJ, Kelly JK 2005. Life history affects the evolution of reproductive isolation among species of Coreopsis (Asteraceae). Evolution 59:112362–69
    [Google Scholar]
  9. Baker H. 1955. Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:3347–49
    [Google Scholar]
  10. Baker RL, Diggle PK. 2011. Node-specific branching and heterochronic changes underlie population-level differences in Mimulus guttatus (Phrymaceae) shoot architecture. Am. J. Bot. 98:121924–34
    [Google Scholar]
  11. Baldwin BG. 2007. Adaptive radiation of shrubby tarweeds (Deinandra) in the California Islands parallels diversification of the Hawaiian silversword alliance (Compositae-Madiinae). Am. J. Bot. 94:2237–48
    [Google Scholar]
  12. Barrett SCH, Harder LD. 2017. The ecology of mating and its evolutionary consequences in seed plants. Annu. Rev. Ecol. Evol. Syst. 48:135–57
    [Google Scholar]
  13. Barrett SCH, Harder LD, Worley AC 1996. The comparative biology of pollination and mating in flowering plants. Philos. Trans. R. Soc. B 351:13451271–80
    [Google Scholar]
  14. Bena G, Lejeune B, Prosperi JM, Olivieri I 1998. Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Proc. R. Soc. B 265:14011141–51
    [Google Scholar]
  15. Bennett MD, Leitch IJ. 2005. Genome size evolution in plants. The Evolution of the Genome TR Gregory 89–162 Cambridge, MA: Academic
    [Google Scholar]
  16. Bergonzi S, Albani MC. 2011. Reproductive competence from an annual and a perennial perspective. J. Exp. Bot. 62:134415–22
    [Google Scholar]
  17. Biere A. 1995. Genotypic and plastic variation in plant size: effects on fecundity and allocation patterns in Lychnis flos-cuculi along a gradient of natural soil fertility. J. Ecol. 83:4629–42
    [Google Scholar]
  18. Billings WD, Mooney HA. 1968. The ecology of arctic and alpine plants. Biol. Rev. 43:4481–529
    [Google Scholar]
  19. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S et al. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:57761040–43
    [Google Scholar]
  20. Boss PK, Thomas MR. 2002. Association of dwarfism and floral induction with a grape “green revolution” mutation. Nature 416:6883847–50
    [Google Scholar]
  21. Bousquet J, Strauss SH, Doerksen AH, Price RA 1992. Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. PNAS 89:167844–48
    [Google Scholar]
  22. Carlquist S. 1974. Island Biology New York: Columbia Univ. Press
  23. Charnov EL, Schaffer WM. 1973. Life-history consequences of natural selection: Cole's result revisited. Am. Nat. 107:958791–93
    [Google Scholar]
  24. Church SA. 2003. Molecular phylogenetics of Houstonia (Rubiaceae): descending aneuploidy and breeding system evolution in the radiation of the lineage across North America. Mol. Phylogenetics Evol. 27:2223–38
    [Google Scholar]
  25. Cole LC. 1954. The population consequences of life history phenomena. Q. Rev. Biol. 29:2103–37
    [Google Scholar]
  26. Datson PM, Murray BG, Steiner KE 2008. Climate and the evolution of annual/perennial life-histories in Nemesia (Scrophulariaceae). Plant Syst. Evol. 270:1–239–57
    [Google Scholar]
  27. Delph LF, Meagher TR. 1995. Sexual dimorphism masks life-history trade-offs in the dioecious plant Silene latifolia. . Ecology 76:3775–85
    [Google Scholar]
  28. Dorken ME, Van Drunen WE 2018. Life-history trade-offs promote the evolution of dioecy. J. Evol. Biol. 31:91405–12
    [Google Scholar]
  29. Duminil J, Hardy OJ, Petit RJ 2009. Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol. Biol. 9:177
    [Google Scholar]
  30. Eagles HA, Cane K, Vallance N 2009. The flow of alleles of important photoperiod and vernalisation genes through Australian wheat. Crop Pasture Sci 60:7646–57
    [Google Scholar]
  31. Eckert CG, Samis KE, Dart S 2006. Reproductive assurance and the evolution of uniparental reproduction in flowering plants. Ecology and Evolution of Flowers LD Harder, SCH Barrett 183–203 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  32. Ehrlén J, Lehtila K. 2002. How perennial are perennial plants. ? Oikos 98:2308–22
    [Google Scholar]
  33. Evans MEK, Hearn D, Hahn WJ, Spangle J, Venable DL 2005. Climate and life-history evolution in evening primroses (Oenothera, Onagraceae): a phylogenetic comparative analysis. Evolution 59:91914–27
    [Google Scholar]
  34. Evans MMS, Poethig RS. 1995. Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol 108:2475–87
    [Google Scholar]
  35. Fiz O, Valcárcel V, Vargas P 2002. Phylogenetic position of Mediterranean Astereae and character evolution of daisies (Bellis, Asteraceae) inferred from nrDNA ITS sequences. Mol. Phylogenetics Evol. 25:1157–71
    [Google Scholar]
  36. Fjellheim S, Boden S, Trevaskis B 2014. The role of seasonal flowering responses in adaptation of grasses to temperate climates. Front. Plant Sci. 5:431
    [Google Scholar]
  37. Friedman J. 2014. Genetic determinants and epistasis for life history trait differences in the common monkeyflower. Mimulus guttatus. J. Hered. 105:6816–27
    [Google Scholar]
  38. Friedman J, Twyford AD, Willis JH, Blackman BK 2015. The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus. Mol. Ecol 24:1111–22
    [Google Scholar]
  39. García MB, Picó FX, Ehrlén J 2008. Life span correlates with population dynamics in perennial herbaceous plants. Am. J. Bot. 95:2258–62
    [Google Scholar]
  40. Geber MA. 1990. The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution 44:4799–819
    [Google Scholar]
  41. Gould BA, Chen Y, Lowry DB 2017. Pooled ecotype sequencing reveals candidate genetic mechanisms for adaptive differentiation and reproductive isolation. Mol. Ecol. 26:1163–77
    [Google Scholar]
  42. Gremer JR, Crone EE, Lesica P 2012. Are dormant plants hedging their bets? Demographic consequences of prolonged dormancy in variable environments. Am. Nat. 179:3315–27
    [Google Scholar]
  43. Gremer JR, Wilcox CJ, Chiono A, Suglia E, Schmitt J 2020. Germination timing and chilling exposure create contingency in life history and influence fitness in the native wildflower Streptanthus tortuosus. J. Ecol 108:1239–55
    [Google Scholar]
  44. Gustafsson A. 1948. Polyploidy, life-form and vegetative reproduction. Hereditas 34:1–21–22
    [Google Scholar]
  45. Hackett WP. 1985. Juvenility, maturation, and rejuvenation in woody plants. Hortic. Rev. 7:109–55
    [Google Scholar]
  46. Ho LST, Ane C. 2014. Phylolm: phylogenetic linear regression. R package version 2.6. https://CRAN.R-project.org/package=phylolm
    [Google Scholar]
  47. Horvitz CC, Schemske DW. 1988. Demographic cost of reproduction in a neotropical herb: an experimental field study. Ecology 69:61741–45
    [Google Scholar]
  48. Hsu C-Y, Liu Y, Luthe DS, Yuceer C 2006. Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:81846–61
    [Google Scholar]
  49. Hughes PW. 2017. Between semelparity and iteroparity: empirical evidence for a continuum of modes of parity. Ecol. Evol. 7:208232–61
    [Google Scholar]
  50. Husband BC. 2000. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proc. R. Soc. B 267:1440217–23
    [Google Scholar]
  51. Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:154–70
    [Google Scholar]
  52. Hyun Y, Richter R, Coupland G 2017. Competence to flower: age-controlled sensitivity to environmental cues. Plant Physiol 173:136–46
    [Google Scholar]
  53. Hyun Y, Vincent C, Tilmes V, Bergonzi S, Kiefer C et al. 2019. A regulatory circuit conferring varied flowering response to cold in annual and perennial plants. Science 363:6425409–12
    [Google Scholar]
  54. Ida TY, Harder LD, Kudo G 2015. The consequences of demand‐driven seed provisioning for sexual differences in reproductive investment in Thalictrum occidentale (Ranunculaceae). J. Ecol. 103:1269–80
    [Google Scholar]
  55. Jensen CS, Salchert K, Nielsen KK 2001. A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiol 125:31517–28
    [Google Scholar]
  56. Johanson U, West J, Lister C, Michaels SD, Amasino RM, Dean C 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:5490344–47
    [Google Scholar]
  57. Kemi U, Niittyvuopio A, Toivainen T, Pasanen A, Quilot-Turion B et al. 2013. Role of vernalization and of duplicated FLOWERING LOCUS C in the perennial Arabidopsis lyrata. . New Phytol 197:1323–35
    [Google Scholar]
  58. Kiefer C, Severing E, Karl R, Bergonzi S, Koch M et al. 2017. Divergence of annual and perennial species in the Brassicaceae and the contribution of cis-acting variation at FLC orthologues. Mol. Ecol. 26:133437–57
    [Google Scholar]
  59. Kim E, Donohue K. 2011. Population differentiation and plasticity in vegetative ontogeny: effects on life-history expression in Erysimum capitatum (Brassicaceae). Am. J. Bot. 98:111752–61
    [Google Scholar]
  60. Kirkendall LR, Stenseth NC. 1985. On defining “breeding once. .” Am. Nat. 125:2189–204
    [Google Scholar]
  61. Knight TM, Steets J, Vamosi JC, Mazer SJ, Burd M et al. 2005. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36:467–97
    [Google Scholar]
  62. Kotoda N, Iwanami H, Takahashi S, Abe K 2006. Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J. Am. Soc. Hortic. Sci. 131:174–81
    [Google Scholar]
  63. Lande R, Schemske DW, Schultz ST 1994. High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution 48:4965–78
    [Google Scholar]
  64. Lazaro A, Obeng-Hinneh E, Albani MC 2018. Extended vernalization regulates inflorescence fate in Arabis alpina by stably silencing PERPETUAL FLOWERING1. . Plant Physiol 176:42819–33
    [Google Scholar]
  65. Lenahan OM, Whiting MD, Elfving DC 2006. Gibberellic acid inhibits floral bud induction and improves “Bing” sweet cherry fruit quality. Hortscience 41:3654–59
    [Google Scholar]
  66. Lesaffre T, Billiard S. 2020. The joint evolution of lifespan and self-fertilization. J. Evol. Biol. 33:141–56
    [Google Scholar]
  67. Lesica P, Young TP. 2005. A demographic model explains life-history variation in Arabis fecunda. Funct. Ecol 19:3471–77
    [Google Scholar]
  68. Lloyd D. 1980. Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytol 86:169–79
    [Google Scholar]
  69. Lloyd D. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153:3370–80
    [Google Scholar]
  70. Lowry DB, Popovic D, Brennan DJ, Holeski LM 2019. Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus. . Evolution 73:61168–81
    [Google Scholar]
  71. Lundgren MR, Des Marais DL 2020. Life history variation as a model for understanding trade-offs in plant-environment interactions. Curr. Biol. 30:4R180–89
    [Google Scholar]
  72. Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C 2011. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. . Plant Physiol 157:41942–55
    [Google Scholar]
  73. Miller AJ, Gross BL. 2011. From forest to field: perennial fruit crop domestication. Am. J. Bot. 98:91389–414
    [Google Scholar]
  74. Moeller DA, Briscoe Runquist RD, Moe AM, Geber MA, Goodwillie C et al. 2017. Global biogeography of mating system variation in seed plants. Ecol. Lett. 20:3375–84
    [Google Scholar]
  75. Mohamed R, Wang C-T, Ma C, Shevchenko O, Dye SJ et al. 2010. Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. . Plant J 62:4674–88
    [Google Scholar]
  76. Monroe JG, Gill B, Turner KG, McKay JK 2019. Drought regimens predict life history strategies in Heliophila. . New Phytol 223:42054–62
    [Google Scholar]
  77. Morgan MT. 2001. Consequences of life history for inbreeding depression and mating system evolution in plants. Proc. R. Soc. B 268:14781817–24
    [Google Scholar]
  78. Morgan MT, Schoen DJ, Bataillon TM 1997. The evolution of self‐fertilization in perennials. Am. Nat. 150:5618–38
    [Google Scholar]
  79. Munoz F, Violle C, Cheptou P-O 2016. CSR ecological strategies and plant mating systems: Outcrossing increases with competitiveness but stress-tolerance is related to mixed mating. Oikos 125:91296–303
    [Google Scholar]
  80. Müntzing A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21:263–378
    [Google Scholar]
  81. Nürk NM, Atchison GW, Hughes CE 2019. Island woodiness underpins accelerated disparification in plant radiations. New Phytol 224:1518–31
    [Google Scholar]
  82. Obeso J. 2002. The costs of reproduction in plants. New Phytol 155:3321–48
    [Google Scholar]
  83. Ogburn RM, Edwards EJ. 2015. Life history lability underlies rapid climate niche evolution in the angiosperm clade Montiaceae. Mol. Phylogenetics Evol. 1:92181–92
    [Google Scholar]
  84. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S et al. 2018. Caper: comparative analyses of phylogenetics and evolution in R. R package version 1.01. https://cran.r-project.org/package=caper
    [Google Scholar]
  85. Ortiz Morea EG, Marques da Silva E, Ferreira e Silva GF, Targino Valente G, Barrera Rojas CH et al. 2016. Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biol 16:40
    [Google Scholar]
  86. Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ et al. 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:3141–47
    [Google Scholar]
  87. Pitelka LF. 1977. Energy allocation in annual and perennial lupines (Lupinus leguminosae). Ecology 58:51055–65
    [Google Scholar]
  88. Primack RB. 1979. Reproductive effort in annual and perennial species of Plantago (Plantaginaceae). Am. Nat. 114:151–62
    [Google Scholar]
  89. Raduski AR, Haney EB, Igić B 2012. The expression of self‐incompatibility in angiosperms is bimodal. Evolution 66:41275–83
    [Google Scholar]
  90. Raunkiær CC. 1934. The Life Forms of Plants and Statistical Plant Geography Oxford, UK: Clarendon
  91. Reekie EG. 1997. Trade-offs between reproduction and growth influence time of reproduction. Plant Resource Allocation FA Bazzaz, J Grace 191–229 San Diego, CA: Academic
    [Google Scholar]
  92. Reekie EG, Bazzaz FA. 1987. Reproductive effort in plants. 3. Effect of reproduction on vegetative activity. Am. Nat. 129:6907–19
    [Google Scholar]
  93. Remington DL, Leinonen PH, Leppälä J, Savolainen O 2013. Complex genetic effects on early vegetative development shape resource allocation differences between Arabidopsis lyrata populations. Genetics 195:31087–102
    [Google Scholar]
  94. Reynolds LK, Stachowicz JJ, Hughes AR, Kamel SJ, Ort BS, Grosberg RK 2017. Temporal stability in patterns of genetic diversity and structure of a marine foundation species (Zostera marina). Heredity 118:4404–12
    [Google Scholar]
  95. Rice A, Smarda P, Novosolov M, Drori M, Glick L et al. 2019. The global biogeography of polyploid plants. Nat. Ecol. Evol. 3:2265–73
    [Google Scholar]
  96. Ricklefs RE, Renner SS. 1994. Species richness within families of flowering plants. Evolution 48:51619–36
    [Google Scholar]
  97. Rohde A, Bhalerao RP. 2007. Plant dormancy in the perennial context. Trends Plant Sci 12:5217–23
    [Google Scholar]
  98. Rubin MJ, Schmid KM, Friedman J 2019. Assortative mating by flowering time and its effect on correlated traits in variable environments. Ecol. Evol. 9:1471–81
    [Google Scholar]
  99. Scofield DG, Schultz ST. 2006. Mitosis, stature and evolution of plant mating systems: low-Φ and high-Φ plants. Proc. R. Soc. B 273:1584275–82
    [Google Scholar]
  100. Shefferson RP, Roach DA. 2010. Longitudinal analysis of Plantago: adaptive benefits of iteroparity in a short-lived, herbaceous perennial. Ecology 91:2441–47
    [Google Scholar]
  101. Silvertown J. 1986. “Biennials”: a reply to Kelly. Am. Nat. 127:5721–24
    [Google Scholar]
  102. Silvertown J. 1989. A binary classification of plant life history and some possibilities for its evolutionary application. Evol. Trends Plants 3:287–90
    [Google Scholar]
  103. Smith SA, Donoghue MJ. 2008. Rates of molecular evolution are linked to life history in flowering plants. Science 322:589886–89
    [Google Scholar]
  104. Soltis DE, Mort ME, Latvis M, Mavrodiev EV, O'Meara BC et al. 2013. Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. Am. J. Bot. 100:5916–29
    [Google Scholar]
  105. Stearns SC. 1992. The Evolution of Life Histories Oxford, UK: Oxford Univ. Press
  106. Stebbins GL. 1950. Variation and Evolution in Plants New York: Columbia Univ. Press
  107. Stinchcombe JR, Weinig C, Ungerer MC, Olsen K, Mays C et al. 2004. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. . PNAS 101:134712–17
    [Google Scholar]
  108. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. . Nature 410:68321116–20
    [Google Scholar]
  109. Tank DC, Olmstead RG. 2008. From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae). Am. J. Bot. 95:5608–25
    [Google Scholar]
  110. Taylor MA, Wilczek AM, Roe JL, Welch SM, Runcie DE et al. 2019. Large-effect flowering time mutations reveal conditionally adaptive paths through fitness landscapes in Arabidopsis thaliana. . PNAS 116:3617890–99
    [Google Scholar]
  111. Tenreira T, Lange MJP, Lange T, Bres C, Labadie M et al. 2017. A specific gibberellin 20-oxidase dictates the flowering-runnering decision in diploid strawberry. Plant Cell 29:92168–82
    [Google Scholar]
  112. Tree of Sex Consort. 2014. Tree of Sex: a database of sexual systems. Sci. Data 1:140015
    [Google Scholar]
  113. Vamosi JC, Otto SP. 2002. When looks can kill: the evolution of sexually dimorphic floral display and the extinction of dioecious plants. Proc. R. Soc. B 269:14961187–94
    [Google Scholar]
  114. Vamosi JC, Otto SP, Barrett SCH 2003. Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. J. Evol. Biol. 16:51006–18
    [Google Scholar]
  115. Van Drunen WE, Husband BC 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytol 224:31266–77
    [Google Scholar]
  116. Vayssières A, Mishra P, Roggen A, Neumann U, Ljung K, Albani MC 2020. Vernalization shapes shoot architecture and ensures the maintenance of dormant buds in the perennial Arabis alpina. . New Phytol 227:199–115
    [Google Scholar]
  117. Venable DL. 2007. Bet hedging in a guild of desert annuals. Ecology 88:51086–90
    [Google Scholar]
  118. Verboom GA, Linder HP, Stock WD 2004. Testing the adaptive nature of radiation: growth form and life history divergence in the African grass genus Ehrharta (Poaceae: Ehrhartoideae). Am. J. Bot. 91:91364–70
    [Google Scholar]
  119. Vico G, Manzoni S, Nkurunziza L, Murphy K, Weih M 2016. Trade-offs between seed output and life span—a quantitative comparison of traits between annual and perennial congeneric species. New Phytol 209:1104–14
    [Google Scholar]
  120. Vos WT, Edwards TJ, van Staden J 1994. Pollination biology of annual and perennial Leonotis species (Lamiaceae). Plant Syst. Evol. 192:1–21–9
    [Google Scholar]
  121. Wadgymar SM, Daws SC, Anderson JT 2017. Integrating viability and fecundity selection to illuminate the adaptive nature of genetic clines. Evol. Lett. 1:126–39
    [Google Scholar]
  122. Wang J-C, Pan B-R, Albach DC 2016. Evolution of morphological and climatic adaptations in Veronica L. (Plantaginaceae). PeerJ 4:e2333
    [Google Scholar]
  123. Wang R, Albani MC, Vincent C, Bergonzi S, Luan M et al. 2011. Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina. . Plant Cell 23:41307–21
    [Google Scholar]
  124. Wang R, Farrona S, Vincent C, Joecker A, Schoof H et al. 2009. PEP1 regulates perennial flowering in Arabis alpina. . Nature 459:7245423–28
    [Google Scholar]
  125. Whittemore AT, Schaal BA. 1991. Interspecific gene flow in sympatric oaks. PNAS 88:62540–44
    [Google Scholar]
  126. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M et al. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. . Science 309:57371056–59
    [Google Scholar]
  127. Wilson WG, Harder LD. 2003. Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy. Am. Nat. 162:2220–41
    [Google Scholar]
  128. Yamaguchi N, Winter CM, Wu M-F, Kanno Y, Yamaguchi A et al. 2014. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. . Science 344:6184638–41
    [Google Scholar]
  129. Young TP, Augspurger CK. 1991. Ecology and evolution of long-lived semelparous plants. Trends Ecol. Evol. 6:9285–89
    [Google Scholar]
  130. Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA et al. 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506:748689–92
    [Google Scholar]
  131. Zhang D-Y. 2000. Resource allocation and the evolution of self-fertilization in plants. Am. Nat. 155:2187–99
    [Google Scholar]
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