Evolutionary significance of seed structure in Alpinioideae (Zingiberaceae)

bs_bs_banner Botanical Journal of the Linnean Society, 2015, 178, 441–466. With 8 figures Evolutionary significance of seed structure in Alpinioideae (Zingiberaceae) 1 Department of Earth & Environmental Sciences, University of Michigan, Ann Arbor, MI 48109-1005, USA 2 Museum of Paleontology, University of Michigan, Ann Arbor, MI 48109-1079, USA 3 Department of Earth Sciences, Royal Holloway, University of London, London TW20 0EX, UK 4 Herbarium, Singapore Botanic Gardens, National Parks Board, Singapore 259569 5 Department of Plant and Microbial Biology & University and Jepson Herbaria, University of California, Berkeley, CA 94720-2465, USA 6 Swiss Light Source, Paul Scherrer Institut, Villigen 5232, Switzerland 7 Advanced Photon Source, Argonne National Laboratories, Argonne, IL 60439, USA 8 Advanced Light Source, Lawrence Berkeley National Laboratories, Berkeley, CA 94720, USA Received 12 March 2014; revised 7 October 2014; accepted for publication 4 January 2015 Alpinioideae is the largest of the four subfamilies of Zingiberaceae and is widely distributed throughout the New and Old World tropics. Recent molecular studies have shown that, although Alpinioideae is a strongly supported monophyletic subfamily with two distinct tribes (Alpinieae and Riedelieae), large genera, such as Alpinia and Amomum, are polyphyletic and are in need of revision. Alpinia and Amomum have been shown to form seven and three distinct clades, respectively, but, for many of these clades, traditional vegetative and floral synapomorphies have not been found. A broad survey of seeds in Alpinioideae using light microscopy and synchrotron-based X-ray tomographic microscopy has shown that many clades have distinctive seed structures that serve as distinctive apomorphies. Tribes Riedelieae and Alpinieae can be distinguished on the basis of operculum structure, with the exception of three taxa analysed. The most significant seed characters were found to be various modifications of the micropylar and chalazal ends, the cell shape of the endotesta and exotesta, and the location of an endotestal gap. A chalazal chamber and hilar rim are reported for the first time in Zingiberaceae. In addition to characterizing clades of extant lineages, these data offer insights into the taxonomic placement of many fossil zingiberalean seeds that are critical to understanding the origin and evolution of Alpinioideae and Zingiberales as a whole. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 441–466. ADDITIONAL KEYWORDS: chalaza – chalazal chamber – embryo – mesotesta – micropyle – operculum – seed – Spirematospermum – synchrotron-based X-ray tomographic microscopy (SRXTM) – testa. INTRODUCTION Zingiberaceae (the gingers) is the largest of the eight families of Zingiberales, and is distributed throughout the Old and New World tropics with a centre of diversity in Asia (Larsen et al., 1998; Larsen, 2005). *Corresponding author. E-mail: The members of the family are easily differentiated from other Zingiberales by a distinct labellum with two fused adaxial staminodes, two nectariferous glands at the base of the style and, perhaps most notably, by the presence of ethereal oils found throughout the vegetative organs of the plant, which give gingers their unique flavour and smell (Kress, 1990; Larsen et al., 1998; Kress et al., 2001; Pedersen, 2003). Traditionally, Zingiberaceae has been divided © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 441–466 441 JOHN C. BENEDICT1*, SELENA Y. SMITH1,2, MARGARET E. COLLINSON3, JANA LEONG-ŠKORNIČKOVÁ4, CHELSEA D. SPECHT5, JULIE L. FIFE6, FEDERICA MARONE6, XIANGHUI XIAO7 and DILWORTH Y. PARKINSON8 442 J. C. BENEDICT ET AL. part, of the fact that many morphological characters used to reconstruct phylogenetic trees or define lineages have been shown to be homoplasious [e.g. presence of bracteoles by Schumann (1904) and labellum shape by Smith (1990a)]. Currently, the most well-known and commonly used morphological characters for taxon identification and phylogenetic reconstruction are those from flowers and inflorescences; however, seed morphology and anatomy are also excellent sources of potentially phylogenetically informative characters (Liao & Wu, 1996, 2000; Tang et al., 2005), and seeds are more readily preserved as fossils than are flowers (e.g. Koch & Friedrich, 1971; Friis, 1988; Manchester & Kress, 1993; Rodriguez-de la Rosa & Cevallos-Ferriz, 1994; Fischer et al., 2009). Several taxonomically useful characters from fruits and seeds have been documented previously for Zingiberales (Grootjen & Bouman, 1981; Manchester & Kress, 1993; Rodriguez-de la Rosa & Cevallos-Ferriz, 1994; Liao & Wu, 1996, 2000; Liao et al., 2004; Tang et al., 2005; Benedict, 2012). In seeds, however, characters derived from the aril, operculum, micropylar collar, perisperm and endosperm, coupled with characters from seed coat anatomy, embryo shape and ovule type, have all been underutilized in understanding phylogenetic relationships and character evolution in the group (Kress et al., 2001, 2002, 2005, 2007). Such characters would not only be useful for the elucidation of relationships and the definition of potential synapomorphies for extant lineages, but would also facilitate the incorporation of fossil taxa into phylogenetic analyses. The first studies of seed and fruit characters in Zingiberales can be traced back to Tschirch (1891), Humphrey (1896), Netolitzky (1926), Mauritzon (1936) and Berger (1958), whose results were summarized, together with other work, by Takhtajan (1985) to give general descriptions of the seed and fruit characters at the family level. Takhtajan (1985) noted that fruits of Zingiberaceae tend to be many seeded, are sometimes fleshy and can be loculicidally, septicidally or irregularly dehiscent. Seeds are most often anatropous, although campylotropous ovules are found in Hedychium J.Koenig. (Zingiberoideae) and orthotropous ovules are found in Cucurma caulina J.Graham (Zingiberoideae; Takhtajan, 1985). Seed coats in Zingiberaceae, and many other taxa in Zingiberales, are formed from the outer integument only (Takhtajan, 1985), and it is here that considerable anatomical variation exists. Takhtajan (1985) noted a range of 5–13 layers of cells that comprise the seed coat, but did not comment on any characters that may be useful for unifying clades in the family. Variation in seed morphology and anatomy in Zingiberaceae has not been well studied, and the only research conducted in a systematic context is that of © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 441–466 into four tribes based on a suite of morphological characters; however, the characters are not uniquely distributed within a single tribe or are not present in all members of the tribe (Kress, Prince & Williams, 2002; Pedersen, 2003). To address this issue, Kress et (...truncated)