View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector South African Journal of Botany 2004, 70(3): 475–487 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY ISSN 0254–6299 Protogyny in Apiaceae, subfamily Apioideae: systematic and geographic distributions, associated traits, and evolutionary hypotheses MA Schlessman1* and FR Barrie2 1 Department of Biology, PO Box 187, Vassar College, 124 Raymond Avenue, Poughkeepsie, New York 12604-0187, United States of America; and Rocky Mountain Biological Laboratory, Crested Butte, Colorado 81224, United States of America 2 Missouri Botanical Garden, PO Box 299, St. Louis, Missouri 63166, United States of America * Corresponding author, e-mail: [email protected] Received 22 April 2003, accepted in revised form 13 November 2003 Apiaceae subfamily Apioideae is characterised by intra- wetter habitats, later flowering times, and eastern or and interfloral dichogamy. There are two distinct pat- transcontinental distributions. The 19 protogynous gen- terns: multicycle protandry and multicycle protogyny. era were all New World endemics characterised by Protogyny is almost completely restricted to New World mostly yellow or purple flowers, the absence of sty- genera. We determined the form of floral dichogamy for lopodia, increasing proportions of staminate flowers in 198 species representing 36 of the 49 genera of sequentially blooming umbels, drier habitats, earlier Apioideae native to North America north of Mexico. We flowering times, and western distributions. The transi- also examined variation in sex expression (proportions tion from protandry to protogyny probably occurred in of perfect and staminate flowers) within and among the late Pliocene, coincident with adaptation to newly plants in populations of 16 species. The form of forming dry grassland and cold desert habitats. The dichogamy was constant among congeners, with the evolutionary forces involved may have included selec- exception of a few adichogamous selfers. The 17 tion for reproductive assurance, pollinator specialisa- protandrous genera included 11 native to both the Old tion, or both. The distinctive patterns of within plant and New Worlds and six endemic to the Americas. The variation in sex expression associated with protandrous protandrous genera were characterised by white flow- and protogynous apioids probably evolved in response ers, the presence of stylopodia, decreasing proportions to floral dichogamy. of staminate flowers in sequentially blooming umbels, Introduction The characteristic leaves, inflorescences and fruits of apioid levels: (1) within perfect flowers (intrafloral), and both (2) umbellifers (Apiaceae subfamily Apioideae), as well as the within and (3) among sequentially blooming umbels (inter- utility of many species, contributed to very early formal floral). In many species, the perfect flowers are protandrous recognition of this well-known taxonomic group (Constance and all flowers within an umbel mature in relative synchrony, 1971). Apioideae inspired Morison’s Plantarum such that both perfect and staminate flowers release pollen Umbelliferarum Distributio Nova, one of the first mono- before the stigmas of perfect flowers become receptive. The graphic works (Hedge 1973), and recent molecular phyloge- different orders of umbels (first order, primary or terminal; netic studies have confirmed that this ‘natural’ group is second order, secondary or lateral; third order, tertiary or indeed monophyletic (Judd et al. 1994, Plunkett et al. 1996, sublateral; etc.) mature sequentially, giving repeated cycles Downie et al. 1998, Downie et al. 2000, Downie et al. 2001). of protandry (Müller 1883, Knuth 1908, Bell 1971, Webb The relative uniformity of apioid floral biology extends well 1981, Lovett Doust and Lovett Doust 1982, Koul et al. 1993). beyond the morphology of inflorescences, flowers and fruits. Following Lloyd and Webb (1986), Schlessman et al. (1990) Other broadly characteristic reproductive traits include self- have described this particular pattern of intra- and interfloral compatibility, andromonoecy, intra- and inter-floral dichogamy as multicycle protandry. Multicycle protandry in dichogamy (sensu Lloyd and Webb 1986), and variation in Apioideae was described by some of the earliest students of sex expression among the sequentially blooming orders of floral biology (Müller 1883, Knuth 1908), and it appears to be umbels borne by individual plants (Bell 1971, Koul et al. ubiquitous in Old World Apioideae. 1993, Schlessman and Graceffa 2001). In sharp contrast to those of the Old World, many New Dichogamy in apioid umbellifers occurs at three structural World apioids exhibit inter- and intrafloral protogyny in a pat- 476 Schlessman and Barrie tern that could be called multicycle protogyny (Foerste 1882, within individual plants, as well as among individuals. We Trelease 1882, Robertson 1888, 1892, Hardin 1929, used JMP™ (SAS Institute 1995) to perform analyses of Schlessman 1978, 1982, Lindsey 1982, 1984, Webb 1984, variance (ANOVAs) with two model effects, plant and umbel Lindsey and Bell 1985, Barrie and Schlessman 1987, order nested within plant. When determining statistical sig- Schlessman and Graceffa 2001). For a number of years, we nificance, we applied the Bonferroni correction for multiple have accumulated data on the systematic distributions of tests of the same hypothesis (Rice 1989). protandry and protogyny in North American Apiaceae. Although we have reported on our work (Barrie and Other traits Schlessman 1987) and shared our data with others (e.g. Bertin 1993, Bertin and Newman 1993), we have not yet When necessary, we consulted Mathias and Constance published. Our purposes here are to report on the systemat- (1944–1945), Pimenov and Leonov (1993), Kartesz (1994), ic distributions of protandry and protogyny among Apioideae regional floras (e.g. Munz 1959, Hitchcock et al. 1961, native to North America (north of Mexico); to examine rela- Fernald 1970, Gleason and Cronquist 1991, Cronquist et al. tionships among the forms of floral dichogamy, biogeogra- 1997), and other literature to determine the geographical phy, phylogeny, and other reproductive traits; and to consid- distributions, durations (annual or perennial), stylopodium er what those relationships suggest about the evolution of morphologies, and flower colours of species. We excluded dichogamy in Apioideae. as non-native those taxa listed as adventive, only cultivated, or escaped from cultivation in North America north of Material and Methods Mexico. We scored the distributions of genera as falling pri- marily east, primarily west, or more or less equally on both Dichogamy sides of the 100th meridian (100°W longitude). The 100th meridian is a convenient general dividing line between the We determined the form of dichogamy by direct observa- more humid eastern United States and the more arid west- tions of plants in the field and herbarium specimens. In the ern United States. Thus, our descriptions of the distributions field, we examined flowers over the range of developmental of species tended to correlate with our categorisations of stages from bud to fruit. We scored perfect flowers as their habitats: dry, mesic (intermediate) or wet. We used protandrous if anthers matured, dehisced and senesced petal colour to describe the colours of flowers. We followed before styles matured (reached maximum length) and stig- Pimenov and Leonov (1993) for names of genera, Kartesz mas appeared receptive (swollen and translucent). We (1994) for names of species, and Downie et al. (2001, scored prefect flowers as protogynous if styles matured, 2003b, Downie, pers. comm.) for the placement of genera in stigmas appeared receptive, and styles senesced before formally or informally recognised monophyletic groups. anthers matured and dehisced. Informed by our field obser- vations, we followed essentially the same protocol in the Results herbarium. We examined herbarium specimens at Colorado State University (CSU), Harvard University Herbaria (GH), Dichogamy the New York Botanical Garden (NY), the University of Montana (MONTU), the University of Texas at Austin (LL, We determined the form of dichogamy for 198 species rep- TEX), Vassar College (VAS), the University of Washington resenting 36 genera, or 70% of the 282 native apioid (WTU), the University of Wyoming (RM), and Washington species, and 73% of the 49 native apioid genera for North State University (WS). When possible, we confirmed our America north of Mexico (Appendix). Dichogamy was uni- general observations by conducting more extensive investi- form within genera, except for the presence of adichogamy gations of our own (e.g. Barrie 1981, Schlessman and in one species each of the otherwise protandrous genera Graceffa 2001) and by consulting the literature. Osmorhiza and Ptilimnium. All 11 genera native to both the New and Old Worlds were protandrous (Appendix part I). In Sex expression contrast, only six of the genera endemic to the New World were protandrous, while 19 were protogynous (Appendix Schlessman sampled populations of 14 apioid umbellifers part II). growing near the Rocky Mountain Biological Laboratory at Gothic (38°57’29”N, 106°59’06”W, elevation 2 926m), which Sex expression is approximately 13km north of the town of Crested Butte in Gunnison County, Colorado, USA. He examined inflores- We documented sex expression for nine protandrous cences