Time-calibrated phylogeny of the woody Australian genus Hakea (Proteaceae) supports multiple origins of insect-pollination among bird-pollinated ancestors

American Journal of Botany

Volumn 99, Issue 3, 2012, Pages 472-487

  Mast, Austin R ^a   Milton, Ethan F ^a   Jones, Eric H ^a   Barker, Robyn M ^b   Barker, William R ^b,c   Weston, Peter H ^d  

^a FLORIDA STATE UNIVERSITY   (United States)

^b State Herbarium of South Australia   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d ROYAL BOTANIC GARDENS AND DOMAIN TRUST   (Australia)

Author keywords

Bird pollination; DNA; Florivory; Hakea; Macadamia: molecular dating; Phylogeny; Proteaceae

Indexed keywords

PLANT DNA;

ANCESTRY; BIRD; CALIBRATION; INSECT; MOLECULAR ANALYSIS; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; POLLINATION; TAXONOMY;

ANIMAL; ARTICLE; AUSTRALIA; BIRD; CLASSIFICATION; GENETICS; INSECT; PHYLOGENY; PHYSIOLOGY; POLLINATION; PROTEACEAE; SPECIES DIFFERENCE; TIME;

ANIMALS; AUSTRALIA; BIRDS; DNA, PLANT; INSECTS; PHYLOGENY; POLLINATION; PROTEACEAE; SPECIES SPECIFICITY; TIME FACTORS;

AVES; HAKEA; HEXAPODA; MACADAMIA; MELIPHAGIDAE; PROTEACEAE;

EID: 84858604125     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100420     Document Type: Article

References (82)

1. AKAIKE, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723.
2. Anderson, C. L., K. BREMER, and E. M. FRIIS. 2005. Dating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points. American Journal of Botany 92: 1737-1748.
3. BARKER, F. K., A. CIBOIS, P. SCHIKLER, J. FEINSTEIN, and J. CRACRAFT. 2004. Phylogeny and diversification of the largest avian radiation. Proceedings of the National Academy of Sciences, USA 101: 11040-11045.
4. BARKER, N. P., P. H. WESTON, F. RUTSCHMANN, and H. SAUQUET. 2007. Molecular dating of the " Gondwanan " plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. Journal of Biogeography 34: 2012-2027.
5. BARKER, R. M., L. HAEGI, and W. R. BARKER. 1999a. Hakea. In A. Wilson [ed.], Flora of Australia, volume 17B, Proteaceae 3, Hakea to Dryandra. 31-170. ABRS/CSIRO, Canberra, Australia.
6. BARKER, W. R., R. M. BARKER, and L. HAEGI. 1999b. Introduction to Hakea. In A. Wilson [ed.], Flora of Australia, volume 17B, Proteaceae 3, Hakea to Dryandra, 1-30. ABRS/CSIRO, Canberra, Australia.
7. BELL, C. D., D. E. SOLTIS, and P. S. SOLTIS. 2005. The age of the angiosperms: A molecular timescale without a clock. Evolution; International Journal of Organic Evolution 59: 1245-1258.
8. BOLES, W. E. 2005. Fossil honeyeaters (Meliphagidae) from the late Tertiary of Riversleigh, north-western Queensland. Emu 105: 21-26.
9. CHand LER, G. T., R. J. BAYER, and M. D. CRISP. 2001. A molecular phylogeny of the endemic Australian genus Gastrolobium (Fabaceae: Mirbelieae) and allied genera using chloroplast and nuclear markers. American Journal of Botany 88: 1675-1687.
10. CRANE, P. R., K. R. PEDERSEN, E. M. F RIIS, and A. N. DRINNAN. 1993. Early Cretaceous (early to middle Albian) platanoid inflorescences associated with Sapindopsis leaves from the Potomac Group of eastern North America. Systematic Botany 18: 328-344.
11. CREPET, W. L., K. C. NIXON, and M. A. Gandolfo. 2004. Fossil evidence and phylogeny: The age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits. American Journal of Botany 91: 1666-1682.
12. CRISP, M., L. COOK, and D. STEANE. 2004. Radiation of the Australian flora: What can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philosophical Transactions of the Royal Society of London, B, Biological Sciences 359: 1551-1571.
13. CRISP, M. D. 1994. Evolution of bird-pollination in some Australian legumes (Fabaceae). In P. Eggleton and R. Vane-Wright [eds.], Phylogenetics and ecology, 281-309. Academic Press, London, UK.
14. CRISP, M. D., G. E. BURROWS, L. G. C OOK, A. H. THORNHILL, and D. M. J. S. BOWMAN. 2011. Flammable biomes dominated by eucalypts originated at the Cretaceous-Palaeogene boundary. Nature Communications 2: 193.
15. CRONK, Q., and I. OJEDA. 2008. Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59: 715-727.
16. DETTMANN, M. E., and D. M. JARZEN. 1998. The early history of the Proteaceae in Australia: The pollen record. Australian Systematic Botany 11: 401-438.
17. DOYLE, J. J. 1992. Gene trees and species trees: Molecular systematics as one-character taxonomy. Systematic Botany 17: 144-163.
18. DRISKELL, A. C., and L. CHRISTIDIS. 2004. Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes, Meliphagidae). Molecular Phylogenetics and Evolution 31: 943-960.
19. DRUMMOND, A. J., S. Y. W. HO, M. J. PHILIPS, and A. RAMBAUT. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: 699-710.
20. EDWARDS, A. W. F. 1972. Likelihood. Cambridge University Press, Cambridge, UK.
21. FAEGRI, K., and L. VAN DER PIJL. 1966. The principles of pollination ecology. Pergamon, Oxford, UK.
22. FITCH, W. M. 1971. Toward defining the course of evolution: Minimum change for a specific tree topology. Systematic Zoology 20: 406-416.
23. FORD, H. A., D. C. PATON, and N. FORDE. 1979. Birds as pollinators of Australian plants. New Zealand Journal of Botany 17: 509-519.
24. FUTUYMA, D. J., and G. MORENO. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19: 207-233.
25. GELMAN, A., and D. B. RUBIN. 1992. Inference from iterative simulation using multiple sequences. Statistical Science 7: 457-472.
26. GILLESPIE, J. H. 1991. The causes of molecular evolution. Oxford University Press, Oxford, UK.
27. GRADSTEIN, F. M., J. G. OGG, and A. G. SMITH. 2004. A geologic time scale. Cambridge University Press, Cambridge, UK.
28. GRANT, V. A. 1994. Historical development of ornithophily in the western North American flora. Proceedings of the National Academy of Sciences, USA 91: 10407-10411.
29. GROOM, P. K., and B. B. LAMONT. 1996. Ecogeographical analysis of Hakea (Proteaceae) in south-western Australia, with special reference to leaf morphology and life form. Australian Journal of Botany 44: 527-542.
30. HANLEY, M. E., B. B. LAMONT, and W. S. ARMBRUSTER. 2009. Pollination and plant defence traits co-vary in Western Australian Hakeas. New Phytologist 182: 251-260.
31. HASEGAWA, M., H. KISHINO, and Y. YANO. 1985. Dating of the human- ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160-174.
32. HOPPER, S. D. 1979. Biogeographical aspects of speciation in the southwest Australian flora. Annual Review of Ecology Evolution and Systematics 10: 399-422.
33. HOPPER, S. D. 1992. Patterns of diversity at the population and species levels in south-west Australian Mediterranean ecosystems. In R. J. Hobbs [ed.], Biodiversity of Mediterranean ecosystems in Australia, 27-46. Surrey Beatty & Sons, Chipping Norton, Australia.
34. JOHNSON, L. A. S., and B. G. BRIGGS. 1975. Proteaceae: evolution and classification of a southern family. Botanical Journal of the Linnean Society 70: 83-182.
35. KHAN, A. M. 1976. Palynology of Tertiary sediments from Papua New Guinea. I. New form genera and species from upper Tertiary sediments. Australian Journal of Botany 24: 753-781.
36. KLUGE, A. G. 1989. A concern for evidence and a phylogenetic hypothesis for relationships among Epicrates (Boidae, Serpentes). Systematic Zoology 38: 7-25.
37. KLUGE, R. L., and S. NESER. 1991. Biological control of Hakea sericea (Proteaceae) in South Africa. Agriculture Ecosystems & Environment 37: 91-113.
38. LECOINTRE, G., and P. DELEPORTE. 2005. Total evidence requires exclusion of phylogenetically misleading data. Zoologica Scripta 34: 101-117.
39. LEWIS, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913-925.
40. LINDER, H. P. 2008. Plant species radiations: Where, when, why? Philosophical Transactions of the Royal Society, B, Biological Sciences 363: 3097-3105.
41. MACPHAIL, M. K., and E. M. TRUSWELL. 1989. Palynostratigraphy of the central west Murray Basin. BMR Journal of Australian Geology and Geophysics 11: 301-331.
42. MADDISON, W. 1995. Phylogenetic histories within and among species. In P. C. Hoch and A. G. Stephenson [eds.], Experimental and molecular approaches to plant biosystematics, 273-287. Missouri Botanical Garden, St. Louis, Missouri, USA.
43. MADDISON, W. P., and D. R. MADDISON. 2005. Ancestral state reconstruction packages for Mesquite, version 1.0. Website http://mesquiteproject.org.
44. MADDISON, W. P., and D. R. MADDISON. 2007. Mesquite: A modular system for evolutionary analysis. Version 2.0. Website http://mesquiteproject.org.
45. MAGALL Ó N, S., P. R. CRANE, and P. S. HERENDEEN. 1999. Phylogenetic pattern, diversity, and diversification of eudicots. Annals of the Missouri Botanical Garden 86: 297-372.
46. MAKINSON, R. O. 2000. Grevillea. In A. J. G. Wilson [ed.], Flora of Australia, volume 17A, Proteaceae 2, Grevillea, 1-524. ABRS/CSIRO, Melbourne, Australia
47. MARTIN, H. A. 1994. Australian Tertiary phytogeography: Evidence from palynology. In R. S. Hill [ed.], History of the Australian vegetation: Cretaceous to Recent, 104-142. Cambridge University Press, Cambridge, UK.
48. MAST, A. R., and T. J. GIVNISH. 2002. Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny. American Journal of Botany 89: 1311-1323.
49. MAST, A. R., E. H. JONES, and S. P. HAVERY. 2005. An assessment of old and new DNA sequence evidence for the paraphyly of Banksia with respect to Dryandra (Proteaceae). Australian Systematic Botany 18: 75-88.
50. MAST, A. R., C. L. WILLIS, E. H. JONES, K. M. DOWNS, and P. H. WESTON. 2008. A smaller Macadamia from a more vagile tribe: Inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae). American Journal of Botany 95: 843-870.
51. MCCALL, A. C., and R. E. IRWIN. 2006. Florivory: The intersection of pollination and herbivory. Ecology Letters 9: 1351-1365.
52. MOOERS, A. O., and D. SCHLUTER. 1999. Reconstructing ancestor states with maximum likelihood: Support for one- and two-rate models. Systematic Biology 48: 623-633.
53. NEI, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York, USA.
54. OLDE, P., and N. MARRIOTT. 1995. The Grevillea book, volume 1. Timber Press, Portland, Oregon, USA.
55. ORCHARD, A. E. 1999. Introduction. In A. E. Orchard [ed.], Flora of Australia, volume 1, Introduction, 2nd ed., 1-10. ABRS/CSIRO, Canberra, Australia.
56. PAGEL, M. 1994. Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London, B, Biological Sciences 255: 37-45.
57. PAGEL, M., and A. M EADE. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist 167: 808-825.
58. PATON, D. C., and H. A. FORD. 1977. Pollination by birds of native plants in South Australia. Emu 77: 73-85.
59. PERRET, M., A. CHAUTEMS, R. SPICHIGER, G. KITE, and V. SAVOLAINEN. 2003. Systematics and evolution of tribe Sinningieae (Gesneriaceae): Evidence from phylogenetic analyses of six plastid DNA regions and nuclear ncpGS. American Journal of Botany 90: 445-460.
60. PHILLIPS, R. D., S. D. HOPPER, and K. W. DIXON. 2010. Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot. Philosophical Transactions of the Royal Society, B, Biological Sciences 365: 517-528.
61. POOT, P., and H. LAMBERS. 2008. Shallow-soil endemics: Adaptive advantages and constraints of a specialized root-system morphology. New Phytologist 178: 371-381.
62. PROCTOR, M., and P. YEO. 1973. The pollination of flowers. Collins, London, UK.
63. RONQUIST, F., and J. P. HUELSENBECK. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19: 1572-1574.
64. SandERSON, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution 19: 101-109.
65. SAUQUET, H., P. H. WESTON, C. L. Anderson, N. P. BARKER, D. J. CANTRILL, A. R. MAST, and V. SAVOLAINEN. 2009. Contrasted patterns of hyperdiversifi cation in Mediterranean hotspots. Proceedings of the National Academy of Sciences, USA 106: 221-225.
66. SIMMONS, M. P. 2004. Independence of alignment and tree search. Molecular Phylogenetics and Evolution 31: 874-879.
67. SLATER, P., P. SLATER, and R. SLATER. 1989. The Slater field guide to Australian birds, revised ed. Reed New Holland, Sydney, New South Wales, Australia.
68. SLOWINSKI, J. B., and R. D. M. P AGE. 1999. How should species phylogenies be inferred from sequence data? Systematic Biology 48: 814-825.
69. SWOFFORD, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, Massachusetts, USA.
70. TAVAR É, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17: 57-86.
71. THORNE, J. L., and H. KISHINO. 2002. Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology 51: 689-702.
72. THORNE, J. L., H. KISHINO, and I. S. PAINTER. 1998. Estimating the rate of evolution of the rate of molecular evolution. Molecular Biology and Evolution 15: 1647-1657.
73. TRIPP, E. A., and P. S. MANOS. 2008. Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution; International Journal of Organic Evolution 62: 1712-1737.
74. WARD, J. V., and J. A. DOYLE. 1994. Ultrastructure and relationships of mid-Cretaceous polyforate and triporate pollen from northern Gondwana. In M. H. Kurmann and J. A. Doyle [eds.], Ultrastructure of fossil spores and pollen, 161-172. Royal Botanic Gardens, Kew, Richmond, UK.
75. WESTON, P. H., and N. P. BARKER. 2006. A new suprageneric classification of the Proteaceae, with an annotated checklist of genera. Telopea 11: 314-344.
76. WHITTALL, J., and M. CARLSON. 2009. Plant defense: A pre-adaptation for pollinator shifts. New Phytologist 182: 5-8.
77. WHITTALL, J. B., and S. A. HODGES. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447: 706-709.
78. WIEGMANN, B. M., D. K. YEATES, J. L. THORNE, and H. KISHINO. 2003. Time flies, a new molecular time-scale for Brachyceran fly evolution without a clock. Systematic Biology 52: 745-756.
79. WILLIAMS, P. A. 1992. Hakea salicifolia - Biology and role in succession in Abel Tasman National Park, New Zealand. Journal of the Royal Society of New Zealand 22: 1-18.
80. YANG, Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. Journal of Molecular Evolution 39: 306-314.
81. YANG, Z. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences 13: 555-556.
82. YOUNG, J. A. 2006. Hakea s of Western Australia: A field and identification guide. J. A. Young, Perth, Australia.