The evolution of life cycles with haploid and diploid phases
Barbara K. Mable and Sarah P. Otto*
Sexual eukaryotic organisms are characterized by an alternation between haploid and diploid phases. In vascular plants and animals, somatic growth and development occur primarily in the diploid phase, with the haploid phase reduced to the gametic cells. In many othereukaryotes, however, growth and development occur in both phases, with substantial variability among organisms in the length of each phase of the life cycle. A number of theoretical models and experimental studies have shed light on factors that may influence life cycle evolution, yet we remain far from a complete understanding of the diversity of life cycles observed in nature. In this paper wereview the current state of knowledge in this field, and touch upon the many questions that remain unanswered. BioEssays 20:453–462, 1998. 1998 John Wiley & Sons, Inc.
Introduction In 1851, Hofmeister1 recognized that plants alternate between two distinct phases, yet it was not until 1894 that Strasburger2 proposed that this ‘‘alternation of generations’’ represented an alternation between haploidand diploid phases.3 Such an alternation of generations is a necessary consequence of sexual reproduction, since a haploid phase must follow meiosis and a diploid phase must follow gamete fusion, but the lengths of these two phases vary widely among organisms.4 This variability is especially pronounced among such organisms as algae and protists, which have life cycles ranging from complete haploiddevelopment to complete diploid development, as illustrated in Figure 1. During the past 20 years, there has been a resurgence of interest in the evolution of life cycles and ploidy levels. However, much of both the theoretical4–15 and experimental16–18 work has concentrated on how and why diploidy has evolved as the dominant state in ‘‘higher’’ plants and animals (reviewed in ref. 19). This focuson the advantages of diploidy has tended to hinder our understanding of the diversity of life cycles seen among organisms and in some cases has resulted in erroneous interpretations of comparative patterns (as argued in ref. 20). Recently, the focus has shifted toward a somewhat more interesting question: why do many eukaryotes (e.g., many protozoa, algae, fungi, mosses, and ferns) maintain analternation of generations in which there is substantial development in both haploid and diploid phases? This shift has led to a number of theoretical predictions about when we might expect to see the evolution of haplonty (somatic development only in the haploid phase), diplonty (somatic development only in the diploid phase), or haploiddiploidy (somatic development in both phases). The purpose ofthis review is to outline the type of variation in life cycles that exists among eukaryotes, summarize theoretical and experimental studies of life cycle evolution, and suggest directions for future research.
Department of Zoology, University of British Columbia, Vancouver, BC, Canada. Contract grant sponsor: NSERC. *Correspondence to: Sarah P. Otto, Department of Zoology, University of BritishColumbia, Vancouver, BC V6T 1Z4, Canada; E-mail: email@example.com, firstname.lastname@example.org
Life cycle variation among eukaryotes The fact that nearly all metazoan taxa undergo somatic development as diploids has strongly shaped our perception of life cycles, leading to a belief in the inherent superiority of the diploid state. One notable exception to complete diplonty is the occurrence ofarrhenotokous animal species, in which haploid males are produced parthenogenetically by diploid females, which are themselves produced sexually (Table 1). Among zoologists, the term ‘‘haplo-diploid’’ is usually reserved to describe taxa with haploid males and diploid females, and so we will use ‘‘haploid–diploid’’ to refer to organisms that alternate between independent haploid and