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The Evolution of Colchicaceae, with a Focus on Chromosome Numbers Author(S): Juliana Chacón, Natalie Cusimano, and Susanne S

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The Evolution of Colchicaceae, with a Focus on Chromosome Numbers Author(S): Juliana Chacón, Natalie Cusimano, and Susanne S The Evolution of Colchicaceae, with a Focus on Chromosome Numbers Author(s): Juliana Chacón, Natalie Cusimano, and Susanne S. Renner Source: Systematic Botany, 39(2):415-427. 2014. Published By: The American Society of Plant Taxonomists URL: http://www.bioone.org/doi/full/10.1600/036364414X680852 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Systematic Botany (2014), 39(2): pp. 415–427 © Copyright 2014 by the American Society of Plant Taxonomists DOI 10.1600/036364414X680852 Date of publication 04/23/2014 The Evolution of Colchicaceae, with a Focus on Chromosome Numbers Juliana Chaco´n,1,2 Natalie Cusimano,1 and Susanne S. Renner1 1Department of Biology, University of Munich, 80638 Munich, Germany. 2Author for correspondence: ([email protected]) Communicating Editor: Mark P. Simmons Abstract—The lily family Colchicaceae consists of geophytic herbs distributed on all continents except the Neotropics. It is particularly diverse in southern Africa, where 80 of the 270 species occur. Colchicaceae exhibit a wide range of ploidy levels, from 2n =14to2n = 216. To understand where and how this cytogenetic diversity arose, we generated multilocus phylogenies of the Colchicaceae and the Colchicum clade that respectively included 85 or 137 species plus relevant outgroups. To infer the kinds of events that could explain the observed numbers in the living species (dysploidy, polyploidization, or demi-duplication, i.e. fusion of gametes of different ploidy), we compared a series of likelihood models on phylograms, penalized likelihood ultrametric trees, and relaxed clock chronograms that con- tained the 58 or 112 species with published chromosome counts. While such models involve simplification and cannot address the processes behind chromosomal rearrangements, they can help frame questions about the direction of change in chromosome numbers in well-sampled groups. The results suggest that dysploidy played a large role in the Colchicaceae, with the exception of Colchicum itself for which we inferred frequent demi-duplication. While it is known that triploids facilitate the fixation of tetraploidy and that plant species often include individuals of odd ploidy level (triploids, pentaploids), we hesitate to accept the phylogenetically inferred scenario without molecular-cytogenetic work and data from experimental hybridizations. Keywords—African Colchicaceae, ancestral chromosome number, maximum likelihood inference, polyploidy. With some 270 species in 15 genera, the Colchicaceae A striking feature of the Colchicaceae is their high karyo- are the third largest family of the Liliales, after the Liliaceae logical variation (Table 1), with chromosome numbers and Smilacaceae. They occur in Africa, Asia, Australasia, ranging from 2n =14(e.g.Uvularia grandiflora;Therman North America and Europe, but not in South or Central and Denniston 1984) to 2n =216(inColchicum corsicum; America (Vinnersten and Manning 2007). Their closest rela- Persson 2009). Such variation contrasts with the sister tives are the Alstroemeriaceae, which have most of their family, Alstroemeriaceae, in which the chromosome num- species in South America (Chaco´n et al. 2012a). Together, bers vary between 2n =16and2n =20(Chaco´netal. the two form the sister clade to the Petermanniaceae, a 2012b: 44 of the 200 species of Alstroemeriaceae have monospecific family restricted to tropical Australia (Vinnersten been counted). The cytogenetics of Colchicum is espe- and Reeves 2003; Fay et al. 2006). All Colchicaceae contain cially complex, with different species having variable colchicine, an alkaloid traditionally used in the treatment chromosome numbers as well as ploidy levels (from tetra- of gout, and also in cytogenetics for its properties as a to 24-ploid; Persson et al. 2011), perhaps related with the microtubule polymerization inhibitor (Vinnersten and Larsson presence of colchicine (Nordenstam 1998). The effect of 2010). Ecologically, Colchicaceae are long-lived cormose or colchicine on the separation of chromosomes after the rhizomatous geophytes with rather large, animal-pollinated anaphase of mitosis was discovered by B. Pernice (1889) flowers offering nectar at the base of their tepals (Nordenstam and described more fully by Eigsti et al. (1945); it revolu- 1998). African Colchicaceae in the Namaqualand desert often tionized cytogenetics because it permitted experimental have leaves with helical shapes and hairy margins that serve doubling of the entire complement of a cell’s chromosome set. to harvest water from dew and fog, which then drips to the Besides by polyploidy, chromosome numbers can change soil and reaches the root zone where it is ultimately stored through chromosome fission (ascending dysploidy) or chro- in the corms (Vogel and Mu¨ller-Doblies 2011). mosome fusion (descending dysploidy; Schubert and Colchicaceae have been the subject of several molecular- Lysak 2011). Polyploidization can represent an evolu- phylogenetic studies that have clarified relationships and tionary dead end (Mayrose et al. 2011), but there is also circumscriptions of the Australian/African genus Wurmbea, abundant evidence of the adaptive success of polyploid the Mediterranean/Irano-Turanian species of the genus populations and the contribution of polyploidy to the for- Colchicum (the latter extending east to Afganistan and mation of new species (Levin 1983; Abbott et al. 2013; Kyrgyzstan; Persson 2007), and the genus Gloriosa, with Weiss-Schneeweiss et al. 2013 and references therein). By 10 species in Africa, India, and southeastern Asia (Vinnersten contrast, dysploidy is thought to arise accidentally, and and Reeves 2003; Vinnersten and Manning 2007). A we know of no proposed adaptive reason for its pre- redefinition of Colchicum to include all ca. 60 species of ponderance in certain clades. Knowing the distribution Androcymbium (distributed in southern and northern Africa of polyploidy and dysploidy in a particular clade or geo- as well as the Mediterranean) was proposed by Manning graphic region can help set up testable hypotheses about et al. (2007) and Persson (2007), while Del Hoyo and evolutionary pathways, for example about the likelihood Pedrola-Monfort (2008) and Del Hoyo et al. (2009) pre- that hybridization played a large role in the recent past. ferred to keep Androcymbium and Colchicum separate. The Here we investigate chromosome number evolution in most comprehensive analysis is that of Thi et al. (2013), the Colchicaceae using the likelihood approach of Mayrose who used patchy matrices of 3 or 6 combined plastid regions et al. (2010), which models the change rates and relative from 70 species, representing most genera, to infer sub- frequencies of several kinds of past events that could plau- family and tribal relationships. sibly explain the observed haploid chromosome numbers 415 416 SYSTEMATIC BOTANY [Volume 39 Table 1. Chromosome numbers available for the Colchicaceae genera (see details of the species and references in the Table S1) Genus No. of species No. of species counted Chromosome number n2n Baeometra Salisb. ex Endl. 1 1 22 Burchardia R. Br. 6 5 48 24 Camptorrhiza Hutch. 2 1 22 Colchicum L. ca. 157 97 14, 18, 20, 21, 22, 24, 27, 32, 40, 42–44, 36, 38, 46, 48, 50, 52, 54, 58, 90, 92, 94, 96, 102, 106, 108, ca. 110, ca. 120, 140, 146, 182, ca. 216 Disporum Salisb. ex G. Don 20 11 14, 16, 18, 30, 32 Gloriosa L. 10 7 20, 21, 22, 44, 66, 88 Hexacyrtis Dinter 1 1 22 Iphigenia Kunth 12 6 11 22 Kuntheria Conran & Clifford 1 1 14 Ornithoglossum Salisb. 8 4 24 Sandersonia Hook. 1 1 24 Shelhammera R. Br. 2 2 14, 36 Tripladenia D. Don 1 1 14 Uvularia L. 5 3 7 14 Wurmbea Thunb. ca. 50 3 14, 20, 40 in a group. The approach requires either a phylogram, that with penalized likelihood (below), and a chronogram obtained under a is, a tree in which branch lengths are proportional to num- relaxed clock model (below) to reconstruct the evolution of chromosome numbers. The first data set included 85 species of Colchicaceae (from bers of DNA substitutions, or an ultrametric tree in which all 15 genera) plus nine outgroups (representing the Alstroemeriaceae, branch lengths are proportional to time. Such ultrametric Petermanniaceae, Ripogonaceae, and Philesiaceae), each sequenced for trees can come from strict clock models or relaxed clock five plastid regions (matK, ndhF, rbcL, rps16, and trnL-F), one mito- models, and they can also be calibrated (typically in mil- chondrial gene (matR), and the internal transcribed spacer of nuclear lion years), in which case the tree is called a time-tree or ribosomal DNA (ITS). Species authors, geographic origin, herbarium voucher specimen,
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