Patterns of evolution in Australian Mimulus and related genera (Phrymaceae~Scrophulariaceae): a molecular phylogeny using chloroplast and nuclear sequence data
Paul M. Beardsley A C and William R. Barker BA Department of Biological Sciences, Idaho State University, Campus Box 8007, Pocatello, ID, 83209, USA.
B State Herbarium of South Australia, Department for Environment and Heritage, PO Box 2732, Kent Town, SA 5071, Australia.
C Corresponding author. Email: bearpau2@isu.edu
Australian Systematic Botany 18(1) 61-73 https://doi.org/10.1071/SB04034
Submitted: 29 July 2004 Accepted: 15 February 2005 Published: 29 March 2005
Abstract
The aim of this work was to develop rigorous phylogenetic hypotheses for the mostly Australian species of Mimulus, Glossostigma, Peplidium, Microcarpaea and Elacholoma (Phrymaceae sensu Beardsley and Olmstead 2002), and to use the phylogeny to explore morphological patterns of evolution. Chloroplast trnL/F and nuclear ribosomal internal and external transcribed spacer sequence data were used to analyse phylogenetic relationships. The results of these analyses confirmed the following conclusions proposed in previous morphological analyses: (1) Glossostigma and Peplidium are supported as monophyletic groups, although support is weak for Peplidium; (2) Australian endemic Elacholoma, in the past of uncertain family placement, is embedded within the same clade as the former two genera despite its unique pair of terete stigmatic lobes; (3) a relatively recent dispersal event from Australia to Iraq and the Middle East for P. maritimum is inferred; (4) a reduction in stamen number from four to two has evolved independently several times in Glossostigma, Peplidium, Microcarpaea and Elacholoma; (5) a switch to an obligately autogamous breeding system has evolved several times independently in the group. New findings include the following: (1) Glossostigma, Peplidium, Microcarpaea and Elacholoma are derived from within Mimulus; (2) Mimulus prostratus is part of a clade that contains Elacholoma and Glossostigma, and this clade is not a part of the same clades as other Mimulus species in Australia; (3) there is some support for Microcarpaea being sister to a clade including Elacholoma, Mimulus prostratus, Glossostigma and Peplidium. The discovery that four mostly Australian genera are derived from within the mostly western North American genus Mimulus has important implications for generic assignments. Phylogenetic interpretations of additional morphological character transformations are discussed.
Acknowledgments
PM Beardsley thanks D Tank, R Olmstead and three anonymous reviewers; and WR Barker thanks the many collectors, field companions and herbaria that have provided material for a prolonged taxonomic revision of the group. Ms Helen Cohn, Librarian of the Royal Botanic Gardens and National Herbarium of Victoria is thanked for promptly providing citation details of several references. This work was supported by an NSF doctoral dissertation grant to PMB.
Argue CL
(1984) Pollen morphology in Dodartia, Lancea, Leucocarpus, and Mazus and an analysis of pollen morphotypes in the Mimuleae (Scrophulariaceae). Canadian Journal of Botany 62, 1287–1297.
Baldwin BG,
Sanderson MJ,
Porter JM,
Wojciechowski MF,
Campbell CS, Donoghue MJ
(1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden 82, 247–277.
Baldwin BG, Markos S
(1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26SrDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10, 449–463.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barker, WR (1981). Scrophulariaceae. In ‘Flora of central Australia’. 4th edn pp. 326–334. (AH and AW Reed: Sydney)
Barker, WR (1982). Evolution and biogeography of arid Australian Scrophulariaceae In ‘Evolution of the flora and fauna of arid Australia’. pp. 286–350. (Peacock Publications: Adelaide)
Barker, WR (1986). Scrophulariaceae. In ‘Flora of South Australia’. pp. 1275–1313. (Government Printer: Adelaide)
Barker, WR (1988). A palynological survey of the Scrophulariaceae. In ‘Abstracts of the 13th International palynological congress, Brisbane’. p. 10.
Barker WR
(1990) New taxa, names and combinations in Lindernia, Peplidium, Stemodia and Striga (Scrophulariaceae), mainly of the Kimberley Region, Western Australia. Journal of the Adelaide Botanical Gardens 13, 79–93.
Barker, WR (1991). A taxonomic revision of Mazus Lour. (Scrophulariaceae) in Australasia. In ‘Aspects of Tasmanian botany—a tribute to Winifred Curtis’. pp. 85–94. (Royal Society of Tasmania: Hobart)
Barker WR
(1992a) New Australian species of Peplidium and Glossostigma (Scrophulariaceae). Journal of the Adelaide Botanic Gardens 15, 71–74.
Barker, WR (1992b). Scrophulariaceae. In ‘Flora of the Kimberley region’. b. pp. 811–839. (Department of Conservation and Land Management: Perth)
Barker, WR (1993). Scrophulariaceae. In ‘List of vascular plants’. 4th edn pp. 80–82. (Botanic Gardens and State Herbarium: Adelaide)
Barker, WR ,
Harden, GJ ,
Briggs, BG ,
Makinson, RO ,
Whalen, AJ ,
and
Wiecek, B (1992). Scrophulariaceae. In ‘Flora of New South Wales’. pp. 552–590. (New South Wales University Press: Sydney)
Barker, WR ,
Harden, GJ ,
Briggs, BG ,
and
Makinson, RO (1999). Scrophulariaceae. In ‘Flora of Victoria’. pp. 483–528. (Inkata Press: Melbourne)
Barker, WR ,
and
Barker, RM (2003). Experiences with systematic studies of large plant genera. (Abstract) In ‘150 National Herbarium of Victoria: celebrating 150 years of plant research in Australia’. pp. 11. (National Herbarium of Victoria: South Yarra, Vic.)
Bean AR
(1997)
Microcarpaea agonis (Scrophulariaceae), a new species from south-eastern Queensland. Austraobaileya 5, 149–151.
Bean AR
(2003) A new species of Mimulus L. (Scrophulariaceae) from Queensland, Australia. Austraobaileya 6, 549–552.
Beardsley PM, Olmstead RG
(2002) Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma.
American Journal of Botany 89, 1093–1102.
Beardsley PM,
Schoenig SE,
Whittall JB, Olmstead RG
(2004) Patterns of evolution in western North American Mimulus (Phrymaceae). American Journal of Botany 91, 474–489.
Bentham, G (1876). Scrophulariaceae. In ‘Genera Plantarum. Vol. 2’. pp. 946–958. (Reeve and Co.: London)
Blake ST
(1959) New or noteworthy plants, chiefly from Queensland, I. Proceedings of the Royal Society of Queensland 70, 33–46.
Bradshaw HD, Schemske DW
(2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176–178.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Burbidge, NT (1963). Dictionary of Australian plant genera gymnosperms and angiosperms. (Angus and Robertson: Sydney)
Burtt BL
(1965) The transfer of Cyrtandromoea from Gesneriaceae to Scrophulariaceae, with notes on the classification of that family. Bulletin of Botanical Surveys of India 7, 73–88.
Cheeseman TF
(1877) Notes on the fertilisation of Glossostigma.
Transactions of the New Zealand Institute 10, 353–356.
Cruden RW
(1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution; International Journal of Organic Evolution 31, 32–46.
Darwin, C (1876). ‘The effects of cross and self fertilisation in the vegetable kingdom’. (John Murray: London)
Doyle JJ, Doyle JL
(1987) A rapid isolation procedure for small quantities of leaf tissue. Phytochemical Bulletin 19, 11–15.
Dumortier, BC (1829). ‘Analyse des familles des plantes, avec l'indication des principaux genres qui s'y rattachent. Vol. 23.’ (Tournay, Hainaut province: Belgium)
Farris JS,
Kallersjo M,
Kluge AG, Bult C
(1994) Testing significance of incongruence. Cladistics 10, 315–319.
| Crossref | GoogleScholarGoogle Scholar |
Felsenstein J
(1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Fenster CB, Ritland K
(1994) Evidence for natural selection on plant mating systems in Mimulus (Scrophulariaceae). International Journal of Plant Sciences 155, 588–596.
| Crossref | GoogleScholarGoogle Scholar |
Fishman L,
Kelly AJ,
Morgan E, Willis JH
(2001) A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159, 1701–1716.
| PubMed |
Fishman L,
Kelly AJ, Willis JH
(2002) Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus.
Evolution; International Journal of Organic Evolution 56, 2138–2155.
| PubMed |
Gilley L, Taberlet P
(1994) The use of chloroplast DNA to resolve plant phylogenies: non-coding versus rbcL sequences. Molecular Biology and Evolution 11, 769–777.
| PubMed |
Grant AL
(1924) A monograph of the genus Mimulus.
Annals of the Missouri Botanical Garden 11, 99–389.
Holtze N
(1898) Notes on the fertilisation of some north Australian plants. Reports of the seventh meeting of the Australian Association for the Advancement of Science. 7, 566–569.
Karron JD,
Mitchell RJ,
Holmquist KG,
Bell JM, Funk B
(2004) The influence of floral display size on selfing rates in Mimulus ringens.
Heredity 92, 242–248.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Karron JD,
Thumser NN,
Tucker R, Hessenauer AJ
(1995) The influence of population density on outcrossing rates in Mimulus ringens.
Heredity 75, 175–180.
Maddison DR
(1991) The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology 40, 315–328.
Mabberley, DJ (1997). ‘The plant-book. A protable dictionary to the vascular plants.’ (Cambridge University Press: Cambridge)
McDade LA, Moody ML
(1999) Phylogenetic relationships among Acanthaceae: evidence from noncoding trnL-trnF chloroplast DNA sequences. American Journal of Botany 86, 70–80.
Müller, H (1883).
von Mueller F
(1895)
Elacholoma Hornii, F.v.M. And Tate. Victorian Naturalist 12, 14–
.
Pennell FW
(1920) Scrophulariaceae of Colombia. Proceedings. Academy of Natural Sciences of Philadelphia 72, 136–188.
Pennell, FW (1935). Scrophulariaceae of eastern temperate North America. In ‘Proceedings of the Academy of Natural Sciences, Philadelphia, Monograph No. 1’. (PA: Wickersham, Lancaster)
Pennell FW
(1947) Some hitherto undescribed Scrophulariaceae of the Pacific states. Proceedings of the Academy of Natural Sciences of Philadelphia 99, 151–171.
Posada D, Crandall KA
(1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schemske DW, Bradshaw HD
(1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences USA 96, 11910–11915.
| Crossref | GoogleScholarGoogle Scholar |
Swofford, DL (1998). ‘PAUP*: phylogenetic analysis using parsimony.’ (Sinauer Associates: Sunderland, MA)
Takebayashi N, Morrell P
(2001) Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. American Journal of Botany 88, 1143–1150.
| PubMed |
Tate R
(1895) A supplement to a census of the flora of extra-tropical South Australia. Transactions of the Royal Society of South Australia 19, 79–83.
Thieret JW
(1954) The tribes and genera of Central American Scrophulariaceae. Ceiba 4, 164–184.
Thieret JW
(1967) Supraspecific classification in the Scrophulariaceae: a review. SIDA Contributions to Botany 3, 87–106.
Thorne RT
(1992) Classification and geography of the flowering plants. Botanical Review 58, 225–348.
von Wettstein, R (1891). Scrophulariaceae. In ‘Die naturlichen Pflanzenfamilien. Vol. 4 (3b)’. pp. 39–107. (Wilhelm Engelmann: Leipzig)
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 |
Whittall JB
(1999) A molecular phylogeny of the Mimulus moschatus alliance (Scrophulariaceae): and its conservation implications. MSc thesis
(Oregon State University:
Corvallis, OR)
Willis JH
(1999) The role of genes of large effect on inbreeding depression in Mimulus guttatus.
Evolution; International Journal of Organic Evolution 53, 1678–1691.
