Palynological characters and their phylogenetic signal in Rubiaceae

Botanical Review, The, July-Sept, 2005 by Steven Dessein, Helga Ochoterena, Petra De Block, Frederic Lens, Elmar Robbrecht, Peter Schols, Erik Smets, Stefan Vinckier, Suzy Huysmans

   I. Abstract
  II. Introduction
 III. Material and Methods
  IV. Results
      A. Pollen Morphological Characteristics of Rubiaceae
         1. Dispersal Unit
         2. Pollen Size
         3. Pollen Shape
         4. Apertures
            a. Number
            b. Position
            c. Type
            d. Protruding Onci and Pollen Buds
         5. Sexine
         6. Nexine Ornamentation
         7. Stratification of the Pollen Wall
      B. Heterostyly and Pollen Dimorphism
      C. Orbicule Characteristics of Rubiaceae
      D. Fossil Pollen Record for Rubiaceae
   V. Discussion
      A. Systematic Significance of Pollen Morphology in Rubiaceae
         1. Subfamily Level
         2. Tribal Level
         3. Generic and Infragenerie Level.
            a. Generic Level
            b. Subgeneric and Specific Level
            c. Infraspecific Variation
      B. Systematic Value of Pollen Data Compared with Other
         Morphological Characters
      C. Orbicules and Phylogeny
      D. Coding Pollen Characters for Cladistic Analyses
  VI. Future Research
 VII. Acknowledgments
VIII. Literature Cited
  IX. Appendix 1: Template for Pollen Descriptions
   X. Appendix 2: List of Genera in the Pollen Database, with
      Reference to the Literature
  XI. Appendix 3: List of Genera according to Tribes

II. Introduction

The predominantly tropical family Rubiaceae includes approximately 12,000 species in 650 genera (Delprete, 1999a), making it one of the five largest families of flowering plants. The publication of Robbrecht's Tropical Woody Rubiaceae (1988a) boosted systematic interest in the family by providing a synthesis of the available morphological data and a comprehensive, worldwide classification system. Since then, many investigators have concentrated their research efforts on Rubiaceae, and a considerable amount of new morphological and molecular data have become available. Mainly due to the advance of molecular systematics, unexpected relationships were often suggested, and the infrafamily classification has changed dramatically to translate the new insights. One of the four subfamilies recognized by Robbrecht (1988a, 1993)--i.e., Antirheoideae--collapsed, and many tribes were redefined (e.g., Isertieae, Naucleeae, Spermacoceae). This process of refining our knowledge of the evolutionary history of Rubiaceae is constantly assisted by morphological observations and continues to date, resulting in shifting genera and tribes, in redelimitation of genera, and in description of new taxa.

Pollen morphological data have proved to be particularly informative in elucidating evolutionary relationships within Rubiaceae. Erdtman's (1952, reprinted in 1971) comparative pollen study of 230 species in 120 genera of Rubiaceae reflected some of the variation. Bremekamp (1952), however, was the pioneer in using pollen characters at a large scale to infer the phylogeny of the family. This is not surprising, because he was also a student of the eurypalynous family Acantaceae, in which he used pollen features to clarify many difficult issues, such as the relationship between Acanthopale C. B. Clarke and Dischistocalyx T. Anders ex Benth., to cite one. Subsequent studies dealing with the systematics of the family often included pollen morphological evidence to support or reject taxonomic decisions (e.g., Bremekamp, 1966; Lewis, 1965a, 1965b; Verdcourt, 1958). Since then, several taxonomists have documented the pollen morphology of their study group, and a few palynological articles have been published at the tribal level, e.g., Morindeae (Johansson, 1987a), Gardenieae (Persson, 1993).

In spite of these efforts, Rubiaceae remained one of the blank spots on the pollen morphological map of flowering plants (Muller, 1981). In the last two decades, however, the input of new observations increased. These new pollen data are scattered over systematic and palynological journals and are often difficult to compare. Moreover, some contributions are not widely accessible, because they are part of unpublished theses (e.g., Es, 1999; Vanthournout, 2002). Because a new synthesis of the pollen morphological knowledge of Rubiaceae was also badly needed, we compiled a database at the Laboratory of Plant Systematics (Catholic University of Leuven), containing key pollen features of Rubiaceae genera with reference to relevant literature. In the present article we portray and discuss the known variation of the main pollen characters. Gaps in our pollen knowledge are localized, and features that deserve more attention are pinpointed. We critically discuss coding issues and measure the power of the phylogenetic signal by evaluating the data on up-to-date evolutionary hypotheses. We also hope that this article will encourage further palynological research in the family and enhance the use of pollen data in phylogenetic analyses.

III. Material and Methods

In order to synthesize the pollen morphology of Rubiaceae, we gathered all of the literature listed in the Seventh Bibliographic Index to the Pollen Morphology of Angiosperms (Tissot & van der Ham, 1994) and added all modern literature. For each genus, we retained the most recent or the most reliable and relevant pollen morphological works. From these, after checking all taxa against the most recent classifications, we distilled the pollen morphological characters at the generic level and stored them in a database with reference to the literature consulted. The pollen database is linked to a systematic database holding basic information such as species number, distribution, and the systematic position of each genus. The database is available online at <http://www.kuleuven.ac.be/bio/sys/pollen>. The quality requirements for the works retained were set as follows: (1) Clear illustrations (preferably SEM and LM photographs) are present; (2) the authors have reliable taxonomic knowledge of the species investigated; (3) pollen descriptions are present or, if not, the main pollen characters can be deduced from the illustrations. Geographically oriented palynological contributions (e.g., pollen floras) or general works on Rubiaceae with scanty notes on pollen morphology were therefore often omitted, but reference to them is made in the database. Genera for which pollen data found in literature do not fulfill the quality requirements set above are present in the database, but they are not used to prepare the pollen description of the tribes to which they belong.