The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms.

 
Abstract 
Introduction 
Types of Cleistogamy 
   Dimorphic Cleistogamy 
   Complete Cleistogamy 
   Induced Cleistogamy 
Occurrence of Cleistogamy 
   Description of Survey 
   Survey Results 
Evolution of Cleistogamy in Angiosperms 
   Phylogenetic Implications 
   Advantages and Disadvantages of CH and CL Flowers 
   Selection for Cleistogamy 
      Variable Environments 
      Inbreeding Depression and Geitonogamy 
      Differential Seed Dispersal 
      Variable Ecological Factors and Plant Size 
Implications for Future Research 
Acknowledgments 
Literature Cited 

Introduction

Cleistogamy, a sexual breeding system defined as the production of permanently closed, self-pollinated flowers, has intrigued botanists for centuries and is now recognized as an important system found in a variety of plant taxa. The term was first used by Kuhn in 1867 to describe bud-like flowers that never opened but yet developed into fruit. He called these cleistogamous flowers (literally, "closed marriage"). Darwin (1877) noted that in a cleistogamous species, these flowers may be the only type produced or they may also appear together on the same plant along with open, typically insect-pollinated flowers (known as chasmogamous or "open marriage" flowers). He described cleistogamy in genera such as Impatiens, Oxalis, and Viola as evidence of natural selection. Cleistogamy was also discussed by Darwin's contemporaries over subsequent decades (e.g., Kerner yon Marilaun, 1902). Since then, many scientists have investigated the ecological, developmental, and evolutionary aspects of cleistogamous (CL) and chasmogamous (CH) flower production in a variety of plant species (e.g., Schemske, 1978; Waller, 1979; Mitchell-Olds & Waller, 1985; Antlfinger, 1986; Schmitt & Ehrhardt, 1987, 1990; McCall et al., 1989; Bennington & McGraw, 1995; Culley, 2002). The production of CH and CL flowers was once thought to be directly analogous to outcrossing and selfing, but CH flowers of some species are now known to occasionally self-pollinate before anthesis via delayed self-pollination (Culley, 2000, 2002) as well as geitonogamy (Stewart, 1994). The number of studies involving species with cleistogamous flowers has risen dramatically in recent years (Fig. 1). Today, cleistogamy is a multifaceted term used to refer to this unique floral type and its subsequent fruits and seeds, and also to the plant species that produce these closed flowers.

[FIGURE 1 OMITTED]

Despite the attention that cleistogamous species have received in the literature, the extent of cleistogamy within angiosperms is still not fully understood. Cleistogamous species and genera have been frequently listed in the literature (Darwin, 1877; Kerner von Marilaun, 1902; Ritzerow, 1908; Rickett, 1932; Uphof, 1938; Camp & Gilly, 1943; Maheshwari, 1962), but the most recent comprehensive reviews of cleistogamy (Connor, 1979; Lord, 1981; Campbell et al., 1983) are well over 20 years old. Furthermore, two of these reviews (Connor, 1979; Campbell et al., 1983) focus strictly on the Poaceae, and a later paper (Plitmann, 1995) focuses on floral dimorphisms in general. There is also some discrepancy in the literature as to what constitutes a cleistogamous species. Confusion may be due to the use of the term "cleistogamy" to refer to species with only CL flowers and to those that produce both CL and CH flower types.

Relative to other breeding systems, the evolution of cleistogamy has received relatively little attention, despite recent advances in molecular techniques that have spurred the development of comprehensive angiosperm phylogenies (e.g., Soltis et al., 2000, 2005; Angiosperm Phylogeny Group, 2003; Hilu et al., 2003). Mapping the cleistogamous trait onto these phylogenies would provide an estimate of the number of times cleistogamy has evolved. The purpose of this review is to (1) clarify the different types of cleistogamy that exist, (2) quantify how often cleistogamy occurs within angiosperm genera and species, (3) estimate the number of times that cleistogamy has evolved within angiosperms, and (4) identify ecological factors that may promote the evolution of cleistogamy in plants.

Types of Cleistogamy