Elizabeth Sheffield

2.1 Introduction

What is meant by the term "alternation of generations'? There is no consensus on this, but a plethora of definitions and interpretations. For example: "The alternation of a sexual phase and an asexual phase in the life cycle of an organism. The two phases, or generations, are often morphologically, and sometimes chromosomally, distinct." This is the current Encyclopedia Britannica version, one of the broadest, and one of the most defensible. One alternative is: "The succession of multicellular haploid and diploid phases in some sexually reproducing organisms . . ." (Purves et al., 2004). The latter is typical of the definitions found in biological textbooks, and as we shall see, restricts the process too much to be useful to fern biologists. The essential feature of the process upon which most authors agree is the presence of distinct multicellular forms. This distinguishes a set of organisms from those with only a single multicellular phase (such as humans, which reproduce, at least at present, via single-celled gametes that, on fusion, generate a multicellular phase morphologically comparable with the parent form that generated the gametes). Organisms with a single multicellular phase include those like ourselves, where the conspicuous phase is diploid ("diplonts"), and those in which the haploid phase is the only one with more than single cells ("haplonts").

The possession of two different free-living forms allows each to exploit different environments. The tiny spores of the ferns allow genes to travel far beyond the immediate vicinity of the parent. As Farrar et al. (Chapter 9) remark, this allows one generation of such organisms to fulfill an exploratory role. It may

Biology and Evolution of Ferns and Lycophytes, ed. Tom A. Ranker and Christopher H. Haufler. Published by Cambridge University Press. © Cambridge University Press 2008.

Figure 2.1 Gemmae - multicellular vegetative propagules formed by gametophytes of some ferns (in this case Vittaria). (LTSEM, scale bar 40 |im.)

turn out that the new environment proves unsuitable for the alternate generation, but some ferns have developed mechanisms to cope with this. For example, many taxa have tough, long-lived gametophytes capable of persisting indefinitely through vegetative growth and proliferation (see Figure 2.1 and Chapter 9).

Although some fern gametophytes may have a greater degree of stress tolerance than the sporophytes of the same species (see Chapter 9 for a review), and most organisms with an alternation produce morphologically distinct forms, this is not always the case. Alternation is not attended by differences in appearance in many algae - described as being isomorphic. It is not immediately obvious why isomorphic life cycles have persisted, as there would seem to be no advantage conferred by alternating between identical life forms. When careful field studies have been undertaken, however, it has become clear that there are significant ecological differences between the two phases of isomorphic species (e.g., Dyck and DeWreede, 1995). Even in the absence of clear-cut differences in ecological requirements of the multicellular stages of isomorphic taxa, there are invariably substantial differences in the cytological and physiological status of their unicellular propagules. Diploid cells have double the DNA and are usually larger than their haploid counterparts, and Cavalier Smith (1978) drew attention to the likely physiological and ecological consequences of size differences for single cells (such as gametes and spores), another factor favoring the maintenance of biphasic life cycles.

Evolution has favored many algae, bryophytes, and fungi with biphasic life cycles characterized by substantial development of both the haploid and diploid phases that generate very different independent organisms (see Bell, 1994), as in the ferns and lycophytes. Such organisms are referred to as heteromorphic. Whether the final form of each generation is similar or entirely different, it seems clear that the biphasic life cycles have persisted since the earliest days of such organisms because they offer opportunities to exploit an environment more efficiently together than either phase could do alone (Hughes and Otto, 1999). They may also reduce the cost of sex. Richerd et al. (1993, 1994) pointed out that if the duration of each phase is equal, biphasic organisms will require sexual union only half as often as haplonts or diplonts. They showed that this intrinsic advantage favors biphasic life cycles whenever the cost of sex is high. The cost is certainly high in organisms unable to ensure that male gametes can be delivered reliably and accurately to female gametes, such as ferns (see Chapters 5 and 9). Mable and Otto (1998) pointed out that this cost can also be reduced through the evolution of asexual reproduction and, as we know (e.g., Moran, 2004) and will see later in this chapter, many ferns also have effective and sophisticated processes to exploit this route.

In summary, the "alternation of generations" refers to a reproductive cycle of certain vascular plants, fungi, and protists in which each phase consists of one of two separate, free-living organisms: a gametophyte, which is often but by no means always genetically haploid, and a sporophyte, which is often, but not always, genetically diploid. The gametophyte generation produces gametes by mitosis. Two gametes, originating from different organisms of the same species or from the same organism, combine to produce a zygote, which is one way to produce a sporophyte generation (see later). This sporophyte produces spores by meiosis, which germinate and develop into gametophytes of the next generation. There are many variations on this theme, but first we need to examine how the literature serves these fundamental steps. In most published work, this takes the form of a diagram and text outlining the "life cycle."

2.2 ''The" fern life cycle

Having written a basic textbook myself, I am only too well aware of the tensions that arise between the need for simplicity and a desire to provide a complete and accurate account. Illustrations of the life cycle of ferns remain dogged with elements that can mislead, however, such as sperm apparently swimming from an antheridium directly into an archegonium from the same gametophyte (e.g., Figure 26.12 in Solomon et al., 2005, Figure 29.13 in Raven et al., 2005, Figure 29.14 in Freeman, 2005, Figure 28.20 in Savada et al., 2008, and Figure 29.11 in Campbell and Reece, 2004). Inclusions in the text do clarify matters in some, for example the last book helpfully includes "Although this illustration shows an egg and sperm from the same gametophyte, a variety of mechanisms promote cross-fertilization between gametophytes." However, the visual presentations in textbooks may leave a long-lasting impression. This is especially worrisome when some illustrators juxtapose gametangia apparently from the same gametophyte in such proximity that the sperm literally have nowhere else to go but into the waiting archegonium (e.g., Figure 29.20 in Purves et al., 2004), so it is good that the figure in the newest edition of the book (Savada et al., 2008) has been re-drawn. However, it is clear that the encouragement given to textbook illustrators in my last review (Sheffield, 1994) to show separate parent gametophytes was largely ignored. I remain convinced that newcomers to the delights of fern life cycles would be better prepared for the genetic consequences of fertilization if life cycles were shown with gametes issuing from more transparently separate parents, as is most certainly the norm in nature (e.g., Ranker et al., 1996; see Chapter 4). Perhaps this would avoid authors trying to figure out fern distributions assuming that they have "small self-fertilizing spores" (e.g., Wild and Gagnon, 2005).

We once needed to turn to specialist literature (e.g., Dyce, 1993) to find helpful examples such as that shown in Figure 2.2. Happily, versions of this have now been adopted by other authors and are starting to appear in the primary literature (e.g., Marrs and Watt, 2006). Figure 2.2 summarizes events in the life cycle of bracken, a fern that does generate butterfly-shaped gametophytes ("prothalli") (see Chapter 9) and routinely forms sporophytes from two separate gametophytes (Wolf et al., 1988; see Figures 2.3 and 2.4). This summary outlines events in Pterid-ium, and should not be assumed to be accurate for other homosporous ferns, or indeed any heterosporous ferns (which seldom receive more than a passing mention in basic textbooks).

2.3 Historical summary

By 1851 Hofmeister had figured out the steps outlined in the fern life cycle just described (see Kaplan and Cooke, 1996, for review). As Mayr (1982) pointed out, it was Hofmeister's insight that all plant life cycles shared common elements that prepared botanists to accept Darwin's principle of common descent. Hofmeister's contribution is seldom recognized, but Farrar et al.

Figure 2.2 Diagram summarizing "the" life cycle of a fern. Taken from Dyce, 1993. (Adapted from Biological Sciences Review, 1 (1988), 36-39, drawn by F. J. Rumsey.)

(Chapter 9) review some of the excellent work that followed, which documented the (at-the-time surprising) role of the gametophyte and the significance of the cytological and morphological changes that attend each stage of the cycle. During the ensuing period, studies of living species and of fossils gradually came together. While paleobotany hardly figured in the punctuated equilibrium debate of the 1970s and 1980s, it has more recently been recognized that fossils, especially those preserved in exquisite detail in beds such as the Rhynie chert, provide insight that allow interpretation of the evolutionary pressures that led to the splendid array of current lycophyte and fern life cycles. Cookso-nia and related early tracheophytes with sporophyte-dominated, heteromorphic life cycles are now thought to have produced all modern day homosporous tra-cheophytes (Gerrienne et al., 2006), whereas at least ten distinct homosporous lineages are thought to have generated heterosporous plants (DiMichele and Bateman, 1996).

Figure 2.3 Whole (inset) and apical region (main picture) of a young gametophyte ("prothallus") of bracken (Pteridium) bearing numerous antheridia. (LTSEM, scale bar 100 | m.)

Efforts to understand the life cycles of the first lycophytes and ferns were at first frustrated by an apparent lack of fossils representing the gamete-producing plants. Thanks to discoveries in the early 1980s, early misinterpretation and assumptions about the ca. 400 million year old plants from which current day lycophytes and ferns arose have gradually been expunged. It is now relatively well accepted that there was an early divergence in vascular plants. The (extinct) rhyniophytes, thought to have represented the earliest vascular land plants, are believed to have been characterized by a more or less isomorphic alternation of generations. Their gametophytes were multilayered, with vascular tissue and a cutinized epidermis, bearing several-centimeter-high gametangiophores (see Taylor et al., 2005, for review). The Eutracheophyta (including all extant vascular plants) probably all had reduced and thalloid gametophytes, having already started the trend towards the heteromorphic, sporophyte-dominant alternation of generations described above (see Gerrienne et al., 2006, for review). It is significant that rhyniophyte gametophytes were unisexual - producing either antheridia or archegonia. Sexual dimorphism in these gametophytes therefore mirrors the situation in present-day lycophytes and ferns, and is inconsistent with earlier models of the bisexual haploid phase of early land plants (rather

Figure 2.4 Whole (inset) and apical region (main picture) of a more mature gametophyte than that shown in Figure 2.3, also bracken (Pteridium), bearing developing and mature archegonia. (LTSEM, scale bar 100 |im.)

like established diagrams of the fern life cycle) (see Taylor et al., 2005, for review).

2.4 Variations on a theme

The regular alternations described so far were historically treated as the "normal" fern and lycophyte life cycle, with departures that avoided one or more of the steps shown in the life cycle regarded as being aberrant or abnormal. The lycophytes and ferns have been pivotal in our understanding that there is more than one way to produce a new generation, and that the changes in ploidy levels that commonly attend the transition from one phase to another need not occur.

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