Heterostyly accelerates diversification via reduced extinction in primroses

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1784, 2014, Pages

  de Vos, Jurriaan M ^a,b   Hughes, Colin E ^a   Schneeweiss, Gerald M ^c   Moore, Brian R ^d   Conti, Elena ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Angiosperm evolution; Heterostyly; Phylogenetic methods; Plant breeding system; Speciation

Indexed keywords

CHLOROPLAST PROTEIN;

DICOTYLEDON; DIVERGENCE; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; EXTINCTION; FLORAL TRAIT; LIFE HISTORY TRAIT; PHYLOGENETICS; POLYMORPHISM; REPRODUCTIVE STRATEGY; SPECIATION (BIOLOGY); SPECIES DIVERSITY;

BIODIVERSITY; DNA SEQUENCE; EVOLUTION; FLOWER; GENETICS; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRIMULACEAE; REPRODUCTION; SPECIES EXTINCTION;

BIODIVERSITY; BIOLOGICAL EVOLUTION; CHLOROPLAST PROTEINS; EXTINCTION, BIOLOGICAL; FLOWERS; GENETICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRIMULACEAE; REPRODUCTION; SEQUENCE ANALYSIS, DNA;

EID: 84902665747     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0075     Document Type: Article

References (85)

1. Mayr E. 1982 The growth of biological thought: diversity, evolution, and inheritance. Cambridge, MA: Harvard University Press.
2. Benton MJ, Emerson BC. 2007 How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology 50, 23-40. (doi:10.1111/j.1475-4983.2006.00612.x)
3. Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A, Rabosky DL, Carnevale G, Harmon LJ. 2009 Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl Acad. Sci. USA 106, 13 410-13 414. (doi:10.1073/ pnas.0811087106)
4. Fiz-Palacios O, Schneider H, Heinrichs J, Savolainen V. 2011 Diversification of land plants: insights from a family-level phylogenetic analysis. BMC Evol. Biol. 11, 341. (doi:10.1186/1471-2148-11-341)
5. Wiegmann BM et al. 2011 Episodic radiations in the fly tree of life. Proc. Natl Acad. Sci. USA 108, 5690-5695. (doi:10.1073/pnas.1012675108)
6. Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC. 2013 Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc. Natl Acad. Sci. USA 110, 1791-1796. (doi:10.1073/pnas. 1209927110)
7. Scotland RW, Sanderson MJ. 2004 The significance of few versus many in the tree of life. Science 303, 643. (doi:10.1126/science.1091483)
8. Rabosky DL, Slater GJ, Alfaro ME. 2012 Clade age and species richness are decoupled across the eukaryotic tree of life. PLoS Biol. 10, e1001381. (doi:10.1371/journal.pbio.1001381.t002)
9. Scheffers BR, Joppa LN, Pimm SL, Laurance WF. 2012 What we know and don't know about Earth's missing biodiversity. Trends Ecol. Evol. 27, 501-510. (doi:10.1016/j.tree.2012.05.008)
10. Crepet WL, Niklas KJ. 2009 Darwin's second 'abominable mystery': why are there so many angiosperm species? Am. J. Bot. 96, 366-381. (doi:10.3732/ajb.0800126)
11. Darwin C. 1903 More letters of Charles Darwin: a record of his work in a series of hitherto unpublished letters. London, UK: John Murray.
12. Crepet WL. 2000 Progress in understanding angiosperm history, success, and relationships: Darwin's abominably 'perplexing phenomenon'. Proc. Natl Acad. Sci. USA 97, 12 939-12 941. (doi:10.1073/pnas.97.24.12939)
13. Vamosi JC, Vamosi SM. 2011 Factors influencing diversification in angiosperms: at the crossroads of intrinsic and extrinsic traits. Am. J. Bot. 98, 460-471. (doi:10.3732/ajb.1000311)
14. Sanderson MJ, Donoghue MJ. 1994 Shifts in diversification rate with the origin of angiosperms. Science 264, 1590-1593. (doi:10.1126/science.264.5165.1590)
15. Smith SA, Beaulieu JM, Stamatakis A, Donoghue MJ. 2011 Understanding angiosperm diversification using small and large phylogenetic trees. Am. J. Bot. 98, 404-414. (doi:10.3732/ajb.1000481)
16. Endress PK. 2011 Changing views of flower evolution and new questions. In Flowers on the tree of life (eds L Wanntorp, LR de Craene), pp. 120-141. Cambridge, UK: Cambridge University Press.
17. Endress PK. 2011 Evolutionary diversification of the flowers in angiosperms. Am. J. Bot. 98, 370-396. (doi:10.3732/ajb.1000299)
18. Kay KM, Sargent RD. 2009 The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annu. Rev. Ecol. Evol. Syst. 40, 637-656. (doi:10.1146/annurev.ecolsys.110308.120310)
19. van der Niet T, Johnson SD. 2012 Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol. Evol. 27, 353-361. (doi:10.1016/j.tree.2012.02.002)
20. Burger WC. 1981 Why are there so many kinds of flowering plants? Bioscience 31, 577-581.
21. Stebbins GL. 1981 Why are there so many species of flowering plants? Bioscience 31, 573-577. (doi:10.2307/1308219)
22. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. 2004 Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35, 375-403. (doi:10.1146/annurev.ecolsys.34.011802.132347)
23. Grant V. 1949 Pollination systems as isolating mechanisms in angiosperms. Evolution 3, 82-97. (doi:10.2307/2405454)
24. Sargent RD. 2004 Floral symmetry affects speciation rates in angiosperms. Proc. R. Soc. Lond. B 271, 603-608. (doi:10.1098/rspb.2003.2644)
25. Hodges SA, Arnold ML. 1995 Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R. Soc. Lond. B 262, 343-348. (doi:10.1098/rspb.1995.0215)
26. Fernandez-Mazuecos M, Blanco-Pastor JL, Gomez JM, Vargas P. 2013 Corolla morphology influences diversification rates in bifid toadflaxes (Linaria sect. Versicolores). Ann. Bot. 112, 1705-1722. (doi:10. 1093/aob/mct214)
27. Stebbins GL. 1970 Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu. Rev. Ecol. Syst. 1, 307-326. (doi:10.1146/annurev.es.01.110170. 001515)
28. Lloyd DG. 1980 Demographic factors and mating patterns in angiosperms. In Botanical monographs 15: demography and evolution in plant populations (ed. OT Solbrig), pp. 67-88. Oxford, UK: Blackwell Scientific Publications.
29. Hamrick JL, Godt M. 1996 Effects of life history traits on genetic diversity in plant species. Phil. Trans. R. Soc. Lond. B 351, 1291-1298. (doi:10. 1098/rstb.1996.0112)
30. Takebayashi N, Morrell PL. 2001 Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88, 1143-1150. (doi:10.2307/3558325)
31. Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igić B. 2010 Species selection maintains self-incompatibility. Science 330, 493-495. (doi:10. 1126/science.1194513)
32. Ferrer MM, Good SV. 2012 Self-sterility in flowering plants: preventing self-fertilization increases family diversification rates. Ann. Bot. 110, 535-553. (doi:10.1093/aob/mcs124)
33. Johnson MTJ, FitzJohn RG, Smith SD, Rausher MD, Otto SP. 2011 Loss of sexual recombination and segregation is associated with increased diversification in evening primroses. Evolution 65, 3230-3240. (doi:10.1111/j.1558-5646.2011.01378.x)
34. Barrett SCH. 1992 Evolution and function of heterostyly. Monogr. Theor. Appl. Genet. 15, 85-127.
35. Naiki A. 2012 Heterostyly and the possibility of its breakdown by polyploidization. Plant Spec. Biol. 27, 3-29. (doi:10.1111/j.1442-1984.2011.00363.x)
36. Darwin C. 1877 The different forms of flowers on plants of the same species. London, UK: John Murray.
37. Ferrero V, Arroyo J, Castro S, Navarro L. 2012 Unusual heterostyly: style dimorphism and selfincompatibility are not tightly associated in Lithodora and Glandora (Boraginaceae). Ann. Bot. 109, 655-665. (doi:10.1093/aob/mcr222)
38. Barrett S, Shore JS. 2008 New insights on heterostyly: comparative biology, ecology and genetics. In Self-incompatibility in flowering plants: evolution, diversity and mechanisms (ed. VE Franklin-Tong), pp. 3-32. Berlin, Germany: Springer.
39. Lewis D, Jones DA. 1992 The genetics of heterostyly. In Evolution and function of heterostyly (ed. SCH Barrett), pp. 129-150. Berlin, Germany: Springer.
40. Keller B, Thomson JD, Conti E. In press. Heterostyly promotes disassortative pollination and reduces sexual interference in Darwin's primroses evidence from experimental studies. Funct. Ecol. (doi:10.1111/ 1365-2435.12274)
41. Armbruster WS, Muchhala N. 2008 Associations between floral specialization and species diversity: cause, effect, or correlation? Evol. Ecol. 23, 159-179. (doi:10.1007/s10682-008-9259-z)
42. Keller B, de Vos JM, Conti E. 2012 Decrease of sexual organ reciprocity between heterostylous primrose species, with possible functional and evolutionary implications. Ann. Bot. 110, 1233-1244. (doi:10.1093/aob/mcs199)
43. Baker HG. 1955 Self-compatibility and establishment after 'long-distance'dispersal. Evolution 9, 347-349. (doi:10.2307/2405656)
44. Källersjö M, Bergqvist G, Anderberg AA. 2000 Generic realignment in primuloid families of the Ericales s.l.: a phylogenetic analysis based on DNA sequences from three chloroplast genes and morphology. Am. J. Bot. 87, 1325-1341. (doi:10.2307/2656725)
45. Mast AR, Kelso S, Richards AJ, Lang DJ, Feller DM, Conti E. 2001 Phylogenetic relationships in Primula L. and related genera (Primulaceae) based on noncoding chloroplast DNA. Int. J. Plant Sci. 162, 1381-1400. (doi:10.1086/323444)
46. Schneeweiss GM, Schönswetter P, Kelso S, Niklfeld H. 2004 Complex biogeographic patterns in Androsace (Primulaceae) and related genera: evidence from phylogenetic analyses of nuclear internal transcribed spacer and plastid trnL-F sequences. Syst. Biol. 53, 856-876. (doi:10.1080/ 10635150490522566)
47. Mast AR, Kelso S, Conti E. 2006 Are any primroses (Primula) primitively monomorphic? New Phytol. 171, 605-616. (doi:10.1111/j.1469-8137.2006.01700.x)
48. Yan HF, He CH, Peng CI, Hu C-M, Hao G. 2010 Circumscription of Primula subgenus Auganthus (Primulaceae) based on chloroplast DNA sequences. J. Syst. Evol. 48, 123-132. (doi:10.1111/j.1759-6831.2010.00068.x)
49. Boucher FC, Thuiller W, Roquet C, Douzet R, Aubert S, Alvarez N, Lavergne S. 2012 Reconstructing the origins of high-alpine niches and cushion life form in the genus Androsace s.l. (Primulaceae). Evolution 66, 1255-1268. (doi:10.1111/j.1558-5646.2011.01483.x)
50. Maddison WP, Midford PE, Otto SP. 2007 Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, 701-710. (doi:10.1080/ 10635150701607033)
51. Guggisberg A, Mansion G, Kelso S, Conti E. 2006 Evolution of biogeographic patterns, ploidy levels, and breeding systems in a diploid-polyploid species complex of Primula. New Phytol. 171, 617-632. (doi:10.1111/j.1469-8137.2006.01722.x)
52. FitzJohn RG. 2012 diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084-1092. (doi:10.1111/j. 2041-210X.2012.00234.x)
53. Chan KMA, Moore BR. 2005 SYMMETREE: whole-tree analysis of differential diversification rates. Bioinformatics 21, 1709-1710. (doi:10.1093/ bioinformatics/bti175)
54. Silvestro D, Schnitzler J, Zizka G. 2011 A Bayesian framework to estimate diversification rates and their variation through time and space. BMC Evol. Biol. 11, 311. (doi:10.1186/1471-2148-11-311)
55. Moore BR, Donoghue MJ. 2009 A Bayesian approach for evaluating the impact of historical events on rates of diversification. Proc. Natl Acad. Sci. USA 106, 4307-4312. (doi:10.1073/pnas.0807230106)
56. Pyron RA, Burbrink FT. 2013 Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses. Trends Ecol. Evol. 28, 729-736. (doi:10.1016/j.tree.2013.09.007)
57. Dixon CJ, Schönswetter P, Vargas P, Ertl S, Schneeweiss GM. 2009 Bayesian hypothesis testing supports long-distance Pleistocene migrations in a European high mountain plant (Androsace vitaliana, Primulaceae). Mol. Phylogenet. Evol. 53, 580-591. (doi:10.1016/j.ympev.2009.07.016)
58. de Vos JM, Wüest RO, Conti E. 2014 Small and ugly? Phylogenetic analyses of the 'selfing syndrome' reveal complex evolutionary fates of monomorphic primrose flowers. Evolution 68, 1042-1057.
59. Richards AJ. 2003 Primula, 2nd edn. Portland, OR: Timber Press.
60. Qiu Y-X, Fu C-X, Comes HP. 2011 Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of quaternary climate and environmental change in the world's most diverse temperate flora. Mol. Phylogenet. Evol. 59, 225-244. (doi:10.1016/j.ympev.2011.01.012)
61. Guggisberg A, Mansion G, Conti E. 2009 Disentangling reticulate evolution in an arctic-alpine polyploid complex. Syst. Biol. 58, 55-73. (doi:10. 1093/sysbio/syp010)
62. Theodoridis S, Randin C, Broennimann O, Patsiou T, Conti E. 2013 Divergent and narrower climatic niches characterize polyploid species of European primroses in Primula sect. Aleuritia. J. Biogeogr. 40, 1278-1289. (doi:10.1111/jbi.12085)
63. Soltis DE et al. 2009 Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336-348. (doi:10. 3732/ajb.0800079)
64. Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH, Otto SP. 2011 Recently formed polyploid plants diversify at lower rates. Science 333, 1257. (doi:10.5061/dryad.6hf21)
65. Vos JM, Keller B, Isham ST, Kelso S, Conti E. 2012 Reproductive implications of herkogamy in homostylous primroses: variation during anthesis and reproductive assurance in alpine environments. Funct. Ecol. 26, 854-865. (doi:10.1111/j.1365-2435.2012.02016.x)
66. Wright SI, Ness RW, Foxe JP, Barrett SC. 2008 Genomic consequences of outcrossing and selfing in plants. Int. J. Plant Sci. 169, 105-118. (doi:10. 1086/523366)
67. Glémin S, Ronfort J. 2013 Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67, 225-240. (doi:10.1111/j.1558-5646.2012.01778.x)
68. Frankham R. 2005 Genetics and extinction. Biol. Conserv. 126, 131-140. (doi:10.1016/j.biocon.2005.05.002)
69. Igić B, Lande R, Kohn JR. 2008 Loss of selfincompatibility and its evolutionary consequences. Int. J. Plant Sci. 169, 93-104. (doi:10.1086/523362)
70. Escobar JS, Cenci A, Bolognini J, Haudry A, Laurent S, David J, Glémin S. 2010 An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64, 2855-2872. (doi:10.1111/ j.1558-5646.2010.01045.x)
71. Benton MJ. 2009 The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323, 728-732. (doi:10.1126/science.1157719)
72. Vamosi JC, Vamosi SM. 2010 Key innovations within a geographical context in flowering plants: towards resolving Darwin's abominable mystery. Ecol. Lett. 13, 1270-1279. (doi:10.1111/j.1461-0248.2010.01521.x)
73. Rosenblum EB et al. 2012 Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. Evol. Biol. 39, 255-261. (doi:10.1007/s11692-012-9171-x)
74. Ferrero V, Rojas D, Vale A, Navarro L. 2012 Delving into the loss of heterostyly in Rubiaceae: is there a similar trend in tropical and non-tropical climate zones? Perspect. Plant Ecol. Evol. Syst. 14, 161-167. (doi:10.1016/j.ppees.2011.11.005)
75. Tippery NP, Les DH. 2011 Phylogenetic relationships and morphological evolution in Nymphoides (Menyanthaceae). Syst. Bot. 36, 1101-1113. (doi:10.1600/036364411X605092)
76. Klak C, Reeves G, Hedderson T. 2004 Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427, 63-65. (doi:10.1038/ nature02243)
77. Cohen JI. 2010 'A case to which no parallel exists': the influence of Darwin's different forms of flowers. Am. J. Bot. 97, 701-716. (doi:10.3732/ajb. 0900395)
78. Wake DB, Wake MH, Specht CD. 2011 Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331, 1032-1035. (doi:10.1126/science.1188545)
79. Moore BR, Donoghue MJ. 2007 Correlates of diversification in the plant clade Dipsacales: geographic movement and evolutionary innovations. Am. Nat. 170(Suppl. 2), S28-S55. (doi:10.1086/519460)
80. Drummond CS, Eastwood RJ, Miotto STS, Hughes CE. 2012 Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling. Syst. Biol. 61, 443-460. (doi:10.1093/sysbio/syr126)
81. Drummond AJ, Rambaut A. 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. (doi:10.1186/1471-2148-7-214)
82. Czaja A. 2003 Paläokarpologische Untersuchungen von Taphozönosen des Unter-und Mittelmiozäns aus dem Braunkohlentagebau Berzdorf/Oberlausitz (Sachsen). Palaeontogr. Abteilung B 265, 1-148.
83. Knobloch E, Mai DH. 1986 Monographie der Früchte und Samen in der Kreide von Mitteleuropa. Rozpravy ústredního ústavu geologickenho, Praha 47, 1-219.
84. Pagel M, Meade A. 2006 BAYESTRAITS. See: http:// www.evolution.rdg.ac.uk/BayesTraits.html.
85. Davis MP, Midford PE, Maddison W. 2013 Exploring power and parameter estimation of the BiSSE method for analyzing species diversification. BMC Evol. Biol. 13, 38. (doi:10. 1186/1471-2148-13-38)