A new explanation for the evolution of pollinia and loss of carpel fusion in Asclepias and the Apocynaceae s.l.

Annals of the Missouri Botanical Garden

Volumn 94, Issue 2, 2007, Pages 474-484

  Wyatt, Robert ^a   Lipow, Sara R ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b OREGON DEPARTMENT OF FORESTRY   (United States)

Author keywords

Apocynaceae; Apocynoideae; Asclepiadoideae; Asclepias; Carpel fusion; Compitum; Late acting self incompatibility; Periplocoideae; Pollinia; Secamonoideae

Indexed keywords

APOCYNACEAE; APOCYNOIDEAE; APOCYNUM; ASCLEPIADOIDEAE; ASCLEPIAS; MAGNOLIOPHYTA; PERIPLOCOIDEAE; RAUVOLFIOIDEAE; SECAMONOIDEAE;

EID: 34547670482     PISSN: 00266493     EISSN: None     Source Type: Journal    
DOI: 10.3417/0026-6493(2007)94[474:ANEFTE]2.0.CO;2     Document Type: Article

References (90)

1. Armbruster, W. S., E. M. Debevec & M. F. Willson. 2002. Evolution of syncarpy in angiosperms: Theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. J. Evol. Biol. 15: 657-672.
2. Arroyo, M. T. K. 1981. Breeding systems and pollination biology in Leguminosae. Pp. 723-769 in R. M. Polhill & P. H. Raven (editors), Advances in Legume Systematics, Part 1. Royal Botanic Gardens, Kew, London.
3. Backlund, M., B. Oxelman & B. Bremer. 2000. Phylogenetic relationships within the Gentianales based on ndhF and rbcL sequences, with particular reference to the Loganiaceae. Amer. J. Bot. 87: 1029-1043.
4. Bawa, K. S. 1974. Breeding systems of trees of a lowland tropical community. Evolution 28: 85-92.
5. _. 1979. Breeding systems of trees in a tropical wet forest. New Zealand J. Bot. 17: 521-524.
6. _, D. H. Perry & J. H. Beach. 1985. Reproductive biology of tropical lowland rain forest trees. 1. Sexual systems and incompatibility mechanisms. Amer. J. Bot. 72: 331-345.
7. Bentham, G. 1876. Ordo CVl. Apocynaceae. Genera Plantarum. Lovell Reeve, London.
8. Bernhardt, P., J. Kenrick & R. B. Knox. 1984. Pollination biology and the breeding system of Acacia retinodes (Leguminosae: Mimosoideae). Ann. Missouri Bot. Gard. 71: 17-29.
9. Brown, R. 1810. On the Asclepiadeae, a natural order of plants separated from the Apocineae of Jussieu. Mem. Wern. Nat. Hist. Soc. 1: 12-78.
10. Broyles, S. B. & R. Wyatt. 1990. Paternity analysis in a natural population of Asclepias exallata: Multiple paternity, functional gender, and the "pollen-donation hypothesis." Evolution 44: 1454-1468.
11. _ & _. 1993. The consequences of self-pollination in Asclepias exaltata, a self-incompatible milkweed. Amer. J. Bot. 80: 41-44.
12. _ & _. 1995. A reexamination of the pollen-donation hypothesis in an experimental population of Asclepias exaltata. Evolution 49: 89-99.
13. Burkhardt, F. & S. Smith (editors). 1990. The Correspondence of Charles Darwin. Cambridge Univ. Press, Cambridge.
14. Copenhaver, G. P. 2005. A compendium of plant species producing pollen tetrads. J. North Carolina Acad. Sci. 121: 17-35.
15. Cruden, R. W. 1977. Pollen-ovule ratios: A conservative indicator of breeding systems in flowering plants. Evolution 31: 32-46.
16. Dannenbaum, C. & R. Schill. 1991. Die Entwicklung der Pollentetraden und Pollinien bei den Asclepiadaceae. Biblioth. Bot. 141: 1-138.
17. de Nettancourt, D. 1977. Incompatibility in Angiosperms. Springer-Verlag, New York.
18. Endlicher, S. L. 1841. Enchiridion Botanicum. Engelmann, Leipzig.
19. Endress, M. E. & P. V. Bruyns. 2000. A revised classification of the Apocynaceae s.l. Bot. Rev. 66: 1-56.
20. Endress, P. K. 1982. Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31: 48-52.
21. _. 1990. Patterns of floral construction in ontogeny and phylogeny. Biol. J. Linn. Soc. 39: 217-225.
22. _. 1994. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge Univ. Press, New York.
23. _, M. Jenny & M. E. Fallen. 1983. Convergent elaboration of apocarpous gynoecia in higher advanced dicotyledons (Sapindales, Malvales, Gentianales). Nordic J. Bot. 3: 293-300.
24. Fallen, M. E. 1985. The gynoecial development and systematic position of Allamanda (Apocynaceae). Amer. J. Bot. 72: 572-579.
25. _. 1986. Floral structure in the Apocynaceae: Morphological, functional, and evolutionary aspects. Bot. Jahrb. Syst. 106: 245-286.
26. Fishbein, M. 2001. Evolutionary innovation and diversification in the flowers of Asclepiadaceae. Ann. Missouri Bot. Gard. 88: 603-623.
27. Gibbs, P. E., P. O. Oliviera & M. B. Bianchi. 1999. Postzygotic control of selfing in Hymenea stigonocarpa (Leguminosae-Caesalpinioideae) , a bat-pollinated tree of the Brazilian cerrados. Int. J. Pl. Sci. 160: 72-78.
28. Gill, D. E. 1989. Fruiting failure, pollinator efficiency, and speciation in orchids. Pp. 458-481 in D. Otte & J. A. Endler (editors), Speciation and Its Consequences. Sinauer Associates, Sunderland, Massachusetts.
29. Gold, J. J. & J. S. Shore. 1995. Multiple paternity in Asclepias syriaca using a paired-fruit analysis. Canad. J. Bot. 73: 1212-1216.
30. Ionta, G. M. & W. S. Judd. 2007. Phylogenetic relationships in Periplocoideae (Apocynaceae s.l.) and insights into the origin of pollinia. Ann. Missouri Bot. Gard. 94: 360-375.
31. Kenrick, J. & R. B. Knox. 1981. Structure and cytochemistry of the stigma and style of Acacia (Mimosaceae). Austral. J. Bot. 29: 733-745.
32. _ & _. 1982. Function of the polyad in reproduction of Acacia. Ann. Bot. 50: 721-727.
33. _, V. Kaul & E. G. Williams. 1986. Self-incompatibility in Acacia retinodes: Site of pollen-tube arrest is the nucellus. Planta 169: 245-250.
34. Kephart, S. R. 1981. Breeding systems in Asclepias incarnata L., A. syriaca L., and A. verticillata L. Amer. J. Bot. 68: 226-232.
35. Knox, R. B. & J. Kenrick. 1983. Polyad function in relation to the breeding system of Acacia. Pp. 441-471 in D. Mulcahy & E. Ottaviano (editors), Pollen: Biology and Implications for Plant Breeding. Elsevier, New York.
36. Koptur, S. 1983. Flowering phenology and floral biology of Inga (Fabaceae: Mimosoideae). Syst. Bot. 8: 354-368.
37. _. 1984. Outcrossing and pollinator limitation of fruit-set: Breeding systems of neotropical Inga trees (Fabaceae: Mimosoideae). Evolution 38: 1130-1143.
38. Kunze, H. 1991. Structure and function in asclepiad pollination. Pl. Syst. Evol. 176: 227-253.
39. _. 1993. Evolution of the translator in Periplocaceae and Asclepiadaceae. Pl. Syst. Evol. 185: 99-102.
40. _. 1996. Morphology of the stamen in the Asclepiadaceae and its systematic relevance. Bot. Jahrb. Syst. 118: 547-579.
41. _ & S. Liede. 1991. Observations on pollination in Sarcostemma (Asclepiadaceae). Pl. Syst. Evol. 178: 95-105.
42. Lahaye, R., J. Klackenberg, M. Källersjö, E. Van Campo & L. Civeyrel. 2007. Phylogenetic relationships between derived Apocynaceae s.l. and within Secamonoideae based on chloroplast sequences. Ann. Missouri Bot. Gard. 94: 376-391.
43. Leeuwenberg, A. J. M. 1994. Taxa of the Apocynaceae above the genus level. Series of revisions of Apocynaceae XXXVIII. Wageningen Agric. Univ. Pap. 94: 45-60.
44. Liede, S. 1996. Anther differentiation in the Asclepiadaceae- Asclepiadeae: Form and function. Pp. 221-235 in W. G. D'Arcy & R. C. Keating (editors), The Anther: Form, Function and Phylogeny. Cambridge Univ. Press, New York.
45. _ & F. Albers. 1994. Tribal disposition of genera in the Asclepiadaceae. Taxon 43: 201-231.
46. Lipow, S. R. 1998. Post-zygotic Self-incompatibility and Self-fertility in the Apocynaceae and Asclepiadaceae. Ph.D. dissertation, Univ. of Georgia, Athens, Georgia.
47. _ & R. Wyatt. 1998. Reproductive biology and breeding system of Gonolobus suberosus (Asclepiadaceae). J. Torrey Bot. Soc. 125: 183-193.
48. _ & _. 1999. Floral morphology and late-acting self-incompatibility in Apocynum cannabinum (Apocynaceae). Pl. Syst. Evol. 219: 99-109.
49. _ & _. 2000. Single gene control of late-acting self-incompatibility in poke milkweed (Asclepias exaltata L.). Genetics 154: 893-907.
50. Livshultz, T., D. J. Middleton, M. E. Endress & J. K. Williams. 2007. Phylogeny of Apocynoideae and the APSA clade (Apocynaceae s.l.). Ann. Missouri Bot. Gard. 94: 324-359.
51. Ly, T. D. 1986. Die Familie Apocynaceae Juss. in Vietnam. Teil 1. Allgemeiner Teil. Feddes Repert. 97: 235-273.
52. Morse, D. H. 1982. The turnover of milkweed pollinia on bumble bees, and implications for outcrossing. Oecologia 53: 187-196.
53. _. 1994. The role of self-pollen in the female reproductive success of common milkweed (Asclepias syriaca: Asclepiadaceae). Amer. J. Bot. 81: 322-330.
54. Nilsson, S., M. E. Endress & E. Grafstrom. 1993. On the relationship of the Apocynaceae and Periplocaceae. Grana (Suppl.) 2: 3-20.
55. Padrutt, J., H. Pellett & P. Ascher. 1992. Postpollination reproductive biology of Rhododendron prinophyllum (Small) Millais. J. Amer. Soc. Hort. Sci. 117: 656-662.
56. Pichon, M. 1948. Classification des Apocynacées. I. Carisées et Ambelaniées. Mém. Mus. Natl. Hist. Nat. 24: 111-181.
57. Pleasants, J. M. 1991. Evidence for short-distance dispersal of pollinia in Asclepias syriaca L. Funct. Ecol. 5: 75-82.
58. Potgieter, K. & V. A. Albert. 2001. Phylogenetic relationships within Apocynaceae s.l. based on trnL intron and trnL-F spacer sequences and propagule characters. Ann. Missouri Bot. Gard. 88: 523-549.
59. Rapini, A., M. W. Chase, D. J. Goyder & J. Griffiths. 2003. Asclepiadeae classification: Evaluating the phylogenetic relationships of New World Asclepiadoideae (Apocynaceae). Taxon 52: 33-50.
60. Rosatti, T. J. 1989. The genera of suborder Apocynineae (Apocynaceae and Asclepiadaceae) in the southeastern United States. J. Arnold Arbor. 70: 307-401.
61. Ruiz-Zapata, T. & M. T. K. Arroyo. 1978. Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10: 221-230.
62. Safwat, F. M. 1962. Floral morphology of Secamone and evolution of the pollinating apparatus in Asclepiadaceae. Ann. Missouri Bot. Gard. 49: 95-129.
63. Sage, T. L. & E. G. Williams. 1993. Self-incompatibility in Asclepias. Pl. Cell Incomp. Newsl. 23: 55-57.
64. _, S. B. Broyles & R. Wyatt. 1990. The relationship between the five stigmatic chambers and two ovaries of milkweed (Asclepias amplexicaulis Sm.) flowers: A three-dimensional assessment. Israel J. Bot. 39: 187-196.
65. _, R. I. Bertin & E. G. Williams. 1994. Ovarian and other late-acting self-incompatibility systems. Pp. 116-140 in E. G. Williams, A. E. Clarke & R. B. Knox (editors), Genetic Control of Self-incompatibility and Reproductive Development in Flowering Plants. Kluwer Academic Publishers, Boston.
66. Schick, B. 1982a. Untersuchungen über die Biotechnik der Apocynaceenblüte. 2. Bau und Funktion des Bestäubungsapparates. Flora 172: 347-371.
67. _. 1982b. Zür Morphologie, Entwicklung, Feinstruktur und Funktion des Translators von Periploca L. (Asclepiadaceae). Trop. Subtrop. Pflanzenwelt 40: 513-553.
68. Schumann, K. 1895. Apocynaceae. Pp. 109-189 in A. Engler & K. Prantl (editors), Die Natürlichen Pflanzenfamilien, Vol. 4(2). Verlag von Wilhelm Engelmann, Leipzig.
69. Sennblad, B. & B. Bremer. 1996. The familial and subfamilial relationships of Apocynaceae and Asclepiadaceae evaluated with rbcL data. Pl. Syst. Evol. 202: 153-175.
70. Simões, A. O., T. Livshultz, E. Conti & M. E. Endress. 2007. Phylogeny and systematics of the Rauvolfioideae (Apocynaceae) based on molecular and morphological evidence. Ann. Missouri Bot. Gard. 94: 268-297.
71. Sparrow, F. K. & N. L. Pearson. 1948. Pollen compatibility in Asclepias syriaca. J. Agric. Res. 77: 187-199.
72. Stebbins, G. L. 1974. Flowering Plants: Evolution above the Species Level. Belknap Press, Cambridge, Massachusetts.
73. Struwe, L., V. A. Albert & B. Bremer. 1994. Cladistics and family level classification of the Gentianales. Cladistics 10: 175-206.
74. van der Pijl, L. & C. H. Dodson. 1966. Orchid Flowers: Their Pollination and Evolution. Univ. Miami Press, Coral Gables, Florida.
75. van Steenis, C. G. G. J. 1969. Plant speciation in Malesia, with special reference to the theory of non-adaptive strategy evolution. Biol. J. Linn. Soc. 1: 97-133.
76. Venter, H. J. T. & R. L. Verhoeven. 1997. A tribal classification of the Periplocoideae (Apocynaceae). Taxon 46: 705-720.
77. Verhoeven, H. J. T. & R. L. Venter. 2001. Pollen morphology of the Periplocoideae, Secamonoideae, and Asclepiadoideae (Apocynaceae). Ann. Missouri Bot. Gard. 88: 569-582.
78. _, S. Liede & M. E. Endress. 2003. The tribal position of Fockea and Cibirhiza (Apocynaceae: Asclepiadoideae): Evidence from pollinium structure and cpDNA sequence data. Grana 42: 70-81.
79. Walker, D. B. 1978. Postgenital carpel fusion in Catharanthus roseus (Apocynaceae). IV. Significance of the fusion. Amer. J. Bot. 65: 119-121.
80. Wilbur, H. M. 1976. Life history evolution in seven milkweeds of the genus Asclepias. J. Ecol. 64: 223-240.
81. Williams, E. G., V. Kaul, J. L. Rouse & R. B. Knox. 1984. Apparent self-incompatibility in Rhododendron ellipticum, R. championae, and R. amiense: A post-zygotic mechanism. Plant Cell Incomp. Newsl. 16: 10-11.
82. Woodson, Jr., R. E. 1930. Studies in the Apocynaceae. I. A critical study of the Apocynoideae (with special reference to the genus Apocynum). Ann. Missouri Bot. Gard. 17: 1-212.
83. _. 1954. The North American species of Asclepias L. Ann. Missouri Bot. Gard. 41: 1-211.
84. Wyatt, R. 1976. Pollination and fruit-set in Asclepias: A reappraisal. Amer. J. Bot. 63: 845-851.
85. _. 1977. Population Dynamics and Reproductive Biology of Butterflyweed, Asclepias tuberosa L. Ph.D. dissertation, Duke Univ., Durham, North Carolina.
86. _ & S. B. Broyles. 1994. Ecology and evolution of reproduction in milkweeds (Asclepias). Annual Rev. Ecol. Syst. 25: 42-441.
87. _, C. T. Ivey & S. R. Lipow. 1996. The breeding system of desert milkweed, Asclepias subulata. Bull. Torrey Bot. Club 123: 180-183.
88. _, A. L. Edwards, S. R. Lipow & C. T. Ivey. 1998. The rare Asclepias texana and its widespread sister species, A. perennis, are self-incompatible and interfertile. Syst. Bot. 23: 151-156.
89. _, S. B. Broyles & S. R. Lipow. 2000. Pollen-ovule ratios in milkweeds (Asclepiadaceae): An exception that probes the rule. Syst. Bot. 25: 171-180.
90. Zomlefer, W. B. 1994. Guide to Flowering Plant Families. Univ. North Carolina Press, Chapel Hill.