Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
Shopping Cart: ( empty )
You are here: Home > Journals > SB > SB07039
RESEARCH ARTICLE
Contents Vol 22(2)

Gender-bending aubergines: molecular phylogenetics of cryptically dioecious Solanum in Australia

Christopher T. Martine A C , Gregory J. Anderson B and Donald H. Les B
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, State University of New York at Plattsburgh, Plattsburgh, NY 12901, USA.

B Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269-3043, USA.

C Corresponding author. Email: christopher.martine@plattsburgh.edu

Australian Systematic Botany 22(2) 107-120 https://doi.org/10.1071/SB07039
Submitted: 17 August 2007  Accepted: 29 January 2009   Published: 30 April 2009

Abstract

The causes, consequences and correlates of dioecy have been the subject of much discussion since the days of Darwin. Several recent authors have stressed the importance of informing this body of theory, with studies focusing on lineages in which both dioecy and hermaphroditism are present. The genus Solanum is an ideal group for analysis, because dioecy, hermaphroditism and potential unisexual transitions (e.g. andromonoecy) among them all occur. Phylogenetic hypotheses are presented for the Australian species in Solanum subgenus Leptostemonum (the ‘spiny solanums’) section Melongena, which contains 10 of the 14 currently described dioecious species in the genus. Phylogenetic analysis of the ITS and trnK–matK gene regions supports a single origin of dioecy from andromonoecy in Australian Solanum. The causes, mechanisms, and maintenance of dioecy in Australian Solanum are explored, including the role of past climate change in the establishment of centres of endemism.


Acknowledgements

The authors thank David E. Symon for providing specimens, discussion and advice; Nicholas Tippery, Norm Wickett, Hilary McManus and Michael Moody for help with laboratory-based aspects of this work; David E. Symon, William R. Barker, Hellmut Toelken and Kym Brennan for extensive field assistance; and Kent Holsinger, Bernard Goffinet, Brigid O’Donnell, Steve Langdon and two anonymous reviewers for comments on the manuscript. Funding was provided by the National Geographic Society, the Elizabeth DeViney Foundation, the American Society of Plant Taxonomists, the Botanical Society of America, the University of Connecticut Center for Conservation and Biodiversity, the University of Connecticut Department of Ecology and Evolutionary Biology, Sigma Xi, PBI Solanum, and the US National Science Foundation.


References


Anderson GJ (1979) Dioecious Solanum of hermaphrodite origin is an example of a broad convergence. Nature 282, 836–838.
| Crossref | GoogleScholarGoogle Scholar | [Accessed 20 March 2006].

Dodson JR, MacPhail MK (2004) Palynological evidence for aridity events and vegetation change during the Middle Pliocene, a warm period in southwestern Australia. Global and Planetary Change 41, 285–307.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Donoghue MJ (1989) Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43, 1137–1156.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Farwig N, Randrianrina EF, Voigt FA, Kraemer M, Bohning-Gaese K (2004) Pollination ecology of the dioecious tree Commiphora guillauminii in Madagascar. Journal of Tropical Ecology 20, 307–316.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Fox JF (1985) Incidence of dioecy in relation to growth form, pollination and dispersal. Oecologia 67, 244–249.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Freeman DC, Doust JL, Elkeblawy A, Miglia KJ, McArthur ED (1997) Sexual specialization and inbreeding avoidance in the evolution of dioecy. Botanical Review 63, 65–92.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ (1980) Ecological constraints on the evolution of breeding systems in seed plants – dioecy and dispersal in gymnosperms. Evolution 34, 959–972.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ (1982) Outcrossing versus ecological constraints in the evolution of dioecy. American Naturalist 119, 849–865.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ, Renner SS (2004) Tropical intercontinental disjunctions: Gondwana breakup, immigration from the boreotropics, and transoceanic dispersal. International Journal of Plant Sciences 165(Suppl.), S1–S6.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London. Series B 351, 1291–1298.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Heilbuth JC (2000) Lower species richness in dioecious clades. American Naturalist 156, 221–241.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Heilbuth JC, Ilves KL, Otto SP (2001) The consequences of dioecy for seed dispersal: modeling the seed-shadow handicap. Evolution 55, 880–888.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Holsinger KE (1993) The evolutionary dynamics of fragmented plant populations. In ‘Biotic interactions and global change’. (Eds P Kareiva, J Kingsolver, R Huey) pp. 198–216. (Sinauer Associates: Sunderland, MA)

Holsinger KE (2000) Demography and extinction in small populations. In ‘Genetics, demography, and the viability of fragmented populations’. (Eds A Young, G Clarke) pp. 55–75. (Cambridge University Press: Cambridge, UK)

Hunziker AT (1960) Estudios sobre Solanaceae II. Sinopsis taxonómica del género Dunalia H.B.K. Boletín de la Academia Nacional de Ciencias 51, 211–244. open url image1

Hunziker AT (2001) ‘Genera Solanacearum: the genera of Solanaceae illustrated, arranged according to a new system.’ (A.R.G. Gantner Verlag K.G.: Ruggell, Liechenstein)

Jaeger P-ML (1985) Systematic studies in the genus Solanum in Africa. PhD Dissertation, University of Birmingham, UK.

Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae. Systematic Botany 19, 143–156.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Kimberley Natural Resource Management Plan (2004) Draft. Rangelands NRM Co-ordinating Group, Kununurra. Available at www.rangelandswa.info/downloads/kim_draft.pdf [Accessed 6 May 2006].

Knapp S, Persson V, Blackmore S (1998) Pollen morphology and functional dioecy in Solanum (Solanaceae). Plant Systematics and Evolution 210, 113–139.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Laffan SW, Crisp MD (2003) Assessing endemism at multiple spatial scales, with an example from the Australian vascular flora. Journal of Biogeography 30, 511–520. open url image1

Les DH, Schneider EL, Padgett DJ, Soltis PS, Soltis DE, Zanis M (1999) Phylogeny, classification and floral evolution of water lilies (Nymphaeaceae: Nymphaeales): a synthesis of non-molecular, rbcL, matK, and 18s rDNA data. Systematic Botany 24, 28–46.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Levin RA, Myers NR, Bohs L (2006) Phylogenetic relationships among the ‘spiny’ solanums (Solanum subgenus Leptostemonum, Solanaceae). American Journal of Botany 93, 157–169.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Levine DA , Anderson GJ (1986) Evolution of dioecy in American Solanum. In ‘Solanaceae: biology and systematics’. (Ed. WG D’Arcy) pp. 264–273. (Columbia University Press: New York)

Lewis D (1942) The evolution of sex in flowering plants. Biological Reviews of the Cambridge Philosophical Society 17, 46–67.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Lewis PO, Holder MT, Holsinger KE (2005) Polytomies and Bayesian phylogenetic inference. Systematic Biology 54, 241–253.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Loveless MD, Hamrick JL, Foster RB (1998) Population structure and mating system in Tachigali versicolor, a monocarpic neotropical tree. Heredity 81, 134–143.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Maddison DR , Maddison WP (2000) ‘MacClade 4: analysis of phylogeny and character evolution.’ (Sinauer Associates: Sunderland, MA)

Martine CT (2006) Two in the bush: on the evolution, distribution and natural history of dioecy in Australian Solanum. PhD Dissertation, University of Connecticut, Storrs, CT.

Martine CT, Anderson GJ (2007) Dioecy, pollination and seed dispersal in Australian spiny Solanum. Acta Horticulturae 745, 269–283. open url image1

Martine CT, Vanderpool D, Anderson GJ, Les DH (2006) Phylogenetic relationships of andromonoecious and dioecious Australian species of Solanum subgenus Leptostemonum section Melongena: inferences from ITS sequence data. Systematic Botany 31, 410–420.
| Crossref | GoogleScholarGoogle Scholar | open url image1

McGlone MS (2005) Goodbye Gondwana. Journal of Biogeography 32, 739–740.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Miller JS, Venable DL (2002) The transition to gender dimorphism on an evolutionary background of self-incompatibility: an example from Lycium (Solanaceae). American Journal of Botany 89, 1907–1915.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Muenchow GE (1987) Is dioecy associated with fleshy fruit? American Journal of Botany 74, 287–293.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Neal PR, Anderson GJ (2005) Are ‘mating systems’ ‘breeding systems’ of inconsistent and confusing terminology in plant reproductive biology? Or is it the other way around? Plant Systematics and Evolution 250, 173–185.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Nix HA , Kalma JD (1972) Climate as a dominant control in the biogeography of Northern Australia and New Guinea. In ‘Bridge and barrier: the natural history and cultural history of Torres Strait’. (Ed. D Walker) pp. 61–91. (Australian National University: Canberra)

Nylander JAA (2002) ‘MrModel Test v1.1: a simplified version of Posada and Crandall’s ModelTest 3.06.’ (Program distributed by the author, Uppsala University, Department of Systematic Zoology: Uppsala, Sweden)

Olmstead RG, Palmer JD (1997) Solanum: implications for phylogeny, classification, and biogeography from cpDNA restriction site variation. Systematic Botany 22, 19–29.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Orthia LA, Crisp MD, Cook LG, deKok RPJ (2005) Bush peas: a rapid radiation with no support for monophyly of Pultenaea (Fabaceae: Mirbelieae). Australian Systematic Botany 18, 133–147.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Pannell J, Barrett SCH (1998) Baker’s law revisited: reproductive assurance in a metapopulation. Evolution 52, 657–668.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Percy DM, Cronk QCB (1997) Conservation in relation to mating system in Nesohedyotis arborea (Rubiaceae), a rare endemic tree from St. Helena. Biological Conservation 80, 135–145.
| Crossref | GoogleScholarGoogle Scholar | open url image1

de Queíroz A (2005) The resurrection of oceanic dispersal in historical biogeography. Trends in Ecology & Evolution 20, 68–73.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. American Journal of Botany 82, 596–606.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Rogstad SH (1992) Saturated NaCl–CTAB solution as a means of field preservation of leaves for DNA analyses. Taxon 41, 701–708.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ross MD (1970) Evolution of dioecy from gynodioecy. Evolution 24, 827–828.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Sawyer NW, Anderson GJ (2000) Dioecy in South American Deprea (Solanaceae). Biotropica 32, 291–298. open url image1

Spies JJ, Minne L, Venter HJT, Venter AM (1993) A cytogenetic study of the functionally dioecious species in the genus Lycium. South African Journal of Botany 59, 535–540. open url image1

Steiner KE (1988) Dioecism and its correlates in the cape flora of South Africa. American Journal of Botany 75, 1742–1754.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Swofford DL (2002) ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.’ (Sinauer Associates: Sunderland, MA)

Symon DE (1979a) Fruit diversity and dispersal in Solanum in Australia. Journal of the Adelaide Botanic Garden 1, 321–331. open url image1

Symon DE (1979 b) Sex forms in Solanum (Solanaceae) and the role of pollen collecting insects. In ‘The biology and taxonomy of Solanaceae’. (Eds JG Hawkes, RN Lester, AD Skelding) pp. 385–397. (Academic Press: London)

Symon DE (1981) A revision of the genus Solanum in Australia. Journal of the Adelaide Botanic Garden 4, 1–367. open url image1

Thomson JD, Barrett SCH (1981) Selection for outcrossing sexual selection and the evolution of dioecy in flowering plants. American Naturalist 118, 443–449.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Thomson JD, Brunet J (1990) Hypotheses for the evolution of dioecy in seed plants. Trends in Ecology & Evolution 5, 11–16.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Vamosi JC, Otto SP (2002) When looks can kill: the evolution of sexually dimorphic floral display and the extinction of dioecious plants. Proceedings of the Royal Society of London. Series B. Biological Sciences 269, 1187–1194.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Vamosi JC, Vamosi SM (2004) The role of diversification in causing the correlates of dioecy. Evolution 58, 723–731.
| PubMed |
open url image1

Vamosi JC, Vamosi SM (2005) Present day risk of extinction may exacerbate the lower species richness of dioecious clades. Diversity & Distributions 11, 25–32.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Vamosi JC, Otto SP, Barrett SCH (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology 16, 1006–1018.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Weese TL, Bohs L (2007) A three-gene phylogeny of the genus Solanum (Solanaceae). Systematic Botany 32, 445–463.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Weiblen GD, Oyama RK, Donoghue MJ (2000) Phylogenetic analysis of dioecy in monocotyledons. American Naturalist 155, 46–58.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weller SG, Sakai AK (1990) The evolution of dicliny in Schiedea (Caryophyllaceae). Heredity 67, 265–273.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Weller SG, Sakai AK (1999) Using phylogenetic approaches for the analysis of plant breeding system evolution. Annual Review of Ecology and Systematics 30, 167–199.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Whalen MD (1984) Conspectus of species groups in Solanum subgenus Leptostemonum. Gentes Herbarum 12, 179–282. open url image1

Whalen MD, Anderson GJ (1981) Distribution of gametophytic self-incompatibility and infrageneric classification in Solanum. Taxon 30, 761–767.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Whalen MD , Costich D (1986) Andromonoecy in Solanum. In ‘Solanaceae: biology and systematics’. (Ed. WG D’Arcy) pp. 284–302. (Columbia University Press: New York)

Wheeler MA, Byrne M (2006) Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia. Australian Journal of Botany 54, 17–26.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

White ME (1990) ‘The flowering of Gondwana.’ (Princeton University Press: Princeton, NJ)

Wilson WG, Harder LD (2003) Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy. American Naturalist 162, 220–241.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora. Bibliotheca Genetica 3, 1–62. open url image1

Yuan Y-M, Wohlhauser S, Möller M, Klackenberg J, Callmander MW, Küpfer P (2005) Phylogeny and biogeography of Exacum (Gentianaceae): a disjunctive distribution in the Indian Ocean Basin resulted from long distance dispersal and extensive radiation. Systematic Biology 54, 21–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zavada MS, Anderson GJ (1997) The wall and aperture development of pollen from dioecious Solanum appendiculatum: what is inaperturate pollen? Grana 36, 129–134. open url image1

Zavada MS , Anderson GJ , Taylor TN (2000) The role of apertures in pollen germination: a case study from Solanum appendiculatum. In ‘Pollen and spores: morphology and biology’. (Eds MM Harley, CM Morton, S Blackmore) pp. 89–97. (Royal Botanic Gardens, Kew: London)










Appendix 1.  List of herbarium vouchers for specimens used for DNA extraction and amplification of the trnK–matK region, plus GenBank accession codes [in brackets]
DNA codes beginning with ‘C’ are deposited at CONN. DNA codes beginning with ‘AU’ are from sheets held at AD and loaned to CTM at CONN. See Martine et al. (2006) for voucher information for ITS sequences
Click to zoom



Appendix 2.  Primers used to amplify the trnK–matK region
All primer dilutions made from stock held in the Les Laboratory, Department of Ecology and Evolutionary Biology, University of Connecticut. Primers designed by Don Les (DL codes) or Nic Tippery (NT codes), unless noted otherwise
Click to zoom