Functional properties of the isomorphic biphasic algal life cycle

Integrative and Comparative Biology, Oct 2006 by Thornber, Carol S

Synopsis

Many species of marine algae have life cycles that involve multiple separate, free-living phases that frequently differ in ploidy levels. These complex life cycles have received increasing scientific attention over the past few decades, due to their usefulness for both ecological and evolutionary studies. I present a synthesis of our current knowledge of the ecological functioning and evolutionary implications of the isomorphic, biphasic life cycles commonly found in many species of marine algae. There are both costs and benefits to life cycles with 2 morphologically similar but separate, free-living phases that differ in ploidy levels (haploids and diploids). Evolutionary theory predicts that the existence of subtle yet important differences between the phases may be what allows these life cycles to be maintained. Different phases of the same species can vary in abundance, in demographic parameters such as mortality and fecundity, in their physiology, and in their resistance to herbivory. Some taxonomic groups within the red algae have received significant attention toward these issues, while our knowledge of these properties for brown and green algae remains limited.

Introduction

Complex life cycles, which involve the existence of more than one stage or phase for a species, are commonly found in a wide variety of marine species, including primary producers, herbivores, and predators. Species with such life cycles face unique ecological and evolutionary constraints, as each and every stage/ phase must be able to survive and/or reproduce for the species to persist. Individuals may undergo dramatic developmental and morphological changes as they age (for example from larval to adult stages, Ebenman 1992; Eckert 2003). Alternatively, other species with complex life cycles such as many algae and plants must cycle through multiple ploidy stages (Niklas 1997). In either case, these stages may occupy similar or different ecological niches and face varying environmental constraints (see review in Santelices 1990). Because these stages are obligately linked to each other, impacts or effects on one stage may cascade through the species' entire life cycle (Gimenez 2006; Marshall and Keough 2006).

An array of multiphasic lifecycles can be found in marine algae (Klinger 1993). Complex life cycles in marine algae are widely distributed across different taxa, including the three groups that contain marine macroalgae: the green (Chlorophyta), the brown (Phaeophyceae), and the red (Rhodophyta) seaweeds. This review is intended to synthesize our existing ecological knowledge of species with biphasic life cycles and provide a perspective of the evolution and maintenance of these life cycles. In particular, I focus on marine macroalgal species with isomorphic biphasic life cycles and our increased understanding of the ecological similarities and differences between apparently identical phases.

Algal life cycles

Most algal life cycles can be separated into 1 of the 3 general categories: gametic (diplontic), zygotic (haplontic), and biphasic (sporic/haplo-diplontic; Bold and Wynne 1985). Species with gametic life cycles consist primarily of diploid organisms, with meiosis occurring at gamete formation; gametes are the only haploid phase and rapidly fuse to create a new diploid zygote (Lee 1999). This is perhaps the most familiar life cycle, as many animals (including humans) have some type of this general life cycle. Species with zygotic life cycles consist primarily of haploid organisms; the only diploid stage is a zygote (from the fusion of two haploid gametes), which rapidly undergoes meiosis to produce new haploid spores or cells. The haploid cells then grow into new gametophytes that, when mature, produce haploid gametes (Lee 1999).

This review focuses on the biphasic life cycle, which is the most complex of the three. It generally involves an obligate cycling between separate, free-living, and independent haploid (gametophyte) and diploid (sporophyte) phases (Figure 1a). Haploid gametes are produced from mature, multicellular haploid gametophytes and released into the water column. Two gametes (usually male and female, but for some green algae the gametes are referred to as and -) then fuse to create a diploid zygote, which settles and then grows into a mature, multicellular diploid sporophyte. Meiosis occurs when haploid spores are formed by the sporophyte; these spores are released into the water column, settle, and then grow into new gametophytes (Lee 1999). Although gametophytes are usually dioecious (separate sexes), as shown in Figure 1a, they are monoecious in some species. This distinction can have important implications for the relative abundance of the 2 phases (see Theoretical predictions).

Most species of red algae have a modified biphasic life cycle, which includes a third, short-lived diploid carposporophyte stage (Figure 1b). This diploid stage is formed by the fusion of haploid gametes on the surface of the female gametophyte thallus (as opposed to both gametes being released and fusing in the water column). This carposporophyte lives attached to the female gametophyte, acquiring nutrients from it (Kamiya and Kawai 2002), and quickly becomes a mass of diploid spores. These diploid carpospores are released into the water column, settle, and become new free-living tetrasporophytes. Tetrasporophytes, when mature, produce haploid tetraspores via meiosis (the prefix tetra is because the spores are packaged in groups of fours). These tetraspores are released into the water column, settle, and grow into male and female haploid gametophytes (Hawkes 1990). This triphasic life cycle is thought to have evolved as a mechanism of increasing reproductive output (Searles 1980), because red algae are unique among algal taxa in lacking flagella on any of their reproductive cells (and thus cannot swim to find a mate). Because these red algal species have life cycles with two independent, free-living phases (although they are technically called "triphasic"), in this review they will be considered together with the other algal species (browns and greens) that have biphasic life cycles. The terms sporophyte and tetrasporophyte will be used to refer to the diploid free-living phase of the life cycle.