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First published online October 23, 2009; doi:10.3732/ajb.0800203 American Journal of Botany 96: 1941-1956 (2009) © 2009 Botanical Society of America, Inc.

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Developmental patterns in anatomy are shared among separate evolutionary origins of stem succulent and storage root-bearing growth habits in Adenia (Passifloraceae)¹

Towson University, Department of Biological Sciences, Baltimore, MD 21252

ABSTRACT

The architecture of flowering plants is astonishingly diverse. To understand evolutionary patterns and processes that account for this diversity, I investigated developmental anatomy of storage roots and stems of 58 species in the genus Adenia (Passifloraceae) using an explicit phylogenetic context. Because expanded storage roots and stem succulence evolved multiple times in Adenia, patterns of transition between succulent and nonsucculent forms were analyzed using a comparative test that accommodates phylogenetic uncertainty. I tested the innervation hypothesis, wherein I expected the evolution of vascular strands to be correlated with evolutionary increases in water storage tissue if evolution of vascular strands facilitates transport through water and starch storage structures. Not only is evolution of vascular strands in stems statistically coupled with evolutionary increases in parenchyma storage tissue, most lineages that evolved expanded storage roots also evolved vascular strands in these roots in parallel to succulent stems. I proposed that vascular strands and closely associated storage parenchyma found in both roots and shoots of Adenia comprise a homologous unit. A switch-like evolutionary mechanism that alters the spatial expression of this unit between roots and shoots can account, in large part, for transitions between markedly different habits such as storage-rooted herbs and succulent-stemmed shrubs.

Key Words: Adenia • Bayesian comparative analysis • cambial variants • growth habit • hypermorphosis • innervation hypothesis • parallelism • Passifloraceae • stem succulence • storage roots • switch-like evolution

Received for publication 21 June 2008. Accepted for publication 2 July 2009.

FOOTNOTES

¹ The author thanks L. McDade, T. Columbus, M. Porter, H. Bell, V. Steinmann, and R. Cerros-Tlatilpa for institutional support, feedback, and instruction with anatomical technique; J. Mauseth, A. Estes, and four anonymous reviewers for helpful criticism and recommendations to improve this manuscript; D. Hannon, J. Trager, E. Specks, C. Hanson, M. Anderson, and A. Razafindratsira for plant samples; and R. Palanivelu and D. Maddison for access to microscopes and digital cameras. The Academy of Natural Sciences also provided microscope time and image composition software. This work was supported by an NSF Doctoral Dissertation Improvement Grant (0105127) and grants from the American Society for Plant Taxonomists, the Cactus and Succulent Society of America, and the Botanical Society of America. Special thanks to Sherwin Carlquist for his generous support.

² Author for correspondence (e-mail: DHearn{at}towson.edu)

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