Species diversity driven by morphological and ecological disparity: a case study of comparative seed morphology and anatomy across a large monocot order

Research Article John C. Benedict*1, Selena Y. Smith1,2, Chelsea D. Specht3, Margaret E. Collinson4,  ckova  5, Dilworth Y. Parkinson6 and Federica Marone7 Jana Leong-Skorni 1 Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI 48109-1005, USA Museum of Paleontology, University of Michigan, Ann Arbor, MI 48109-1079, USA 3 Department of Plant and Microbial Biology, Integrative Biology and the University and Jepson Herbaria, University of California, Berkeley, CA 94750-2465, USA 4 Department of Earth Sciences, Royal Holloway University of London, London TW20 0EX, UK 5 Herbarium, Singapore Botanic Gardens, National Parks Board, 259569 Singapore 6 Advanced Light Source, Lawrence Berkeley National Labs, Berkeley, CA 94720, USA 7 Swiss Light Source, Paul Scherrer Institut, 5232 Villigen PSI, Switzerland 2 Received: 31 March 2016; Accepted: 17 August 2016; Published: 4 September 2016 Associate Editor: Joseph Williams  ckova  J, Parkinson DY, Marone F. 2016. Species diversity Citation: Benedict JC, Smith SY, Specht CD, Collinson ME, Leong-Skorni driven by morphological and ecological disparity: a case study of comparative seed morphology and anatomy across a large monocot order. AoB PLANTS 8: plw063; doi:10.1093/aobpla/plw063 Abstract. Phenotypic variation can be attributed to genetic heritability as well as biotic and abiotic factors. Across Zingiberales, there is a high variation in the number of species per clade and in phenotypic diversity. Factors contributing to this phenotypic variation have never been studied in a phylogenetic or ecological context. Seeds of 166 species from all eight families in Zingiberales were analyzed for 51 characters using synchrotron based 3D X-ray tomographic microscopy to determine phylogenetically informative characters and to understand the distribution of morphological disparity within the order. All families are distinguishable based on seed characters. Non-metric multidimensional scaling analyses show Zingiberaceae occupy the largest seed morphospace relative to the other families, and environmental analyses demonstrate that Zingiberaceae inhabit both temperate and tropical regions, while other Zingiberales are almost exclusively tropical. Temperate species do not cluster in morphospace nor do they share a common suite of character states. This suggests that the diversity seen is not driven by adaptation to temperate niches; rather, the morphological disparity seen likely reflects an underlying genetic plasticity that allowed Zingiberaceae to repeatedly colonize temperate environments. The notable morphoanatomical variety in Zingiberaceae seeds may account for their extraordinary ecological success and high species diversity as compared to other Zingiberales. Keywords: Cannaceae; Costaceae; Heliconiaceae; Lowiaceae; Marantaceae; Musaceae; Strelitziaceae; Species diversity driven by morphological and ecological disparity: a case study of comparative seed morphology and anatomy across a large monocot order Zingiberaceae. * Corresponding author’s e-mail address: C The Authors 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. V This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS www.aobplants.oxfordjournals.org C The Authors 2016 V 100 Benedict et al. — Zingiberales seed morphoanatomy Introduction 002 AoB PLANTS www.aobplants.oxfordjournals.org C The Authors 2016 V Understanding what processes account for the diversity of life on Earth is a fundamental question in biology. There are a myriad of factors and influences that contribute to the genotypic and phenotypic diversity of a taxon, including the complex evolutionary histories within and between species, the array of ecological space that a taxon inhabits and the overall developmental and genetic variation that provide the raw material for the evolution of new forms and functions (Cowling et al., 1996; Baldwin and Sanderson, 1998; Barrier et al., 1999). Documenting the morphological and anatomical diversity of organisms through time, incorporating data from both extant organisms and their extinct ancestors preserved in the fossil record, is fundamental to understanding diversity. By drawing correlations between current mechanisms of selection and those that may have been acting in the past, such studies can begin to address the tempo and mode of phenotypic changes that have occurred from deep time through to the present. This includes how past organisms may have responded to environmental variables or have developed ecological tolerances. Within angiosperms, the Zingiberales (bananas, gingers and relatives) are a large monophyletic order of monocotyledonous plants that serve as a model group for understanding the mechanisms underlying diversity through time (Kress and Specht, 2005). Based on molecular sequence data, the Zingiberales underwent a proposed rapid radiation in the Cretaceous (Kress and Specht, 2006; Sass et al., 2016), resulting in the eight families of the order. Out of ca. 2500 extant species in the order, the number of species varies substantially from seven in Strelitziaceae to ca. 1600 in Zingiberaceae (The Plant List, 2013). Likewise, the phenotypic diversity of the eight families varies widely with respect to floral, vegetative and anatomical characters as well as diversity of life history strategies and environmental/ecological ranges (Kress and Specht, 2005, 2006). The Zingiberales are found primarily in the tropics and subtropics worldwide (Kress et al., 2001) and form a wellsupported clade based on molecular and morphological characters. The order has been informally divided into two groups, the monophyletic ‘ginger group’ (Zingiberaceae, Costaceae, Marantaceae and Cannaceae) which is supported by several apomorphies, and the paraphyletic ‘banana group’ (Musaceae, Strelitziaceae, Lowiaceae and Heliconiaceae; Kress and Specht, 2005; Simpson, 2010; Sass et al., 2016; Fig. 1). Previous studies have addressed the genetic basis for floral diversity in the group (Specht and Bartlett, 2009; Bartlett and Specht, 2010, 2011; Specht et al., 2012). In addition, the family Zingiberaceae has been shown to possess very morphologically diverse seed and embryo structures (Benedict et al., 2015a, b), but less is known about seed diversity in the other families of the order. An understanding of seed structural diversity will contribute to our ability to untangle the complex evolutionary history of this economically and ecologically important group of plants by allowing inclusion and reevaluation of fossils, and, more broadly, to explore what factors independently influence the diversity of different lineages. While many anatomical and developmental st (...truncated)