Prospects & Overviews
Karl J. Niklas1), Edward D. Cobb1) and Ulrich Kutschera2) Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for spontaneous whole-genome duplication (autopolyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition.
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Keywords: algae; alternation of generations; auto-polyploidy; chiasmata; embryophytes; meiosis; syngamy
Introduction In his Systema Naturae, Carl Linnaeus (1707–1778) placed all plants with hidden reproductive organs into a class he called “Cryptogamae” [1], a group that included fungi, lichens,
DOI 10.1002/bies.201400045 1)
2)
Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA Institute of Biology, University of Kassel, Kassel, Germany
*Corresponding author: Karl J. Niklas E-mail: [email protected]
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algae, bryophytes, and pteridophytes. Although the German bryologist Johannes Hedwig (1730–1799) had discovered structures he attributed to sexual reproduction, the life cycle of early-divergent land plants (e.g. mosses and ferns) remained enigmatic until the publication of a remarkable monograph written by Wilhelm Hofmeister (1824–1877), who summarized his discoveries during the 1840s concerning the modes of reproduction of cryptogams [2]. In this monograph, Hofmeister concluded that the land plant life cycles had an alternation of two generations in which germinating spores develop into plants bearing sperm-producing antheridia and egg-producing archegonia (the gametophyte). After fertilization by sperm, the gametophytes produce plants that develop into a second multicellular generation (the sporophyte) that ultimately gives rise to the next generation of spores [2]. Thus, Hofmeister asserted the homology of land plant gametophytes and sporophytes. Over 40 years later, Eduard Strasburger (1844–1912) proposed that the land plant life cycle involved an alternation between a haploid gametophytic phase and a diploid sporophytic phase [3]. Despite these early insights, much of the evolution of the life cycles and reproduction remains unknown or problematic [4–8]. Here, we explore these topics in the hope of providing an additional perspective on the evolution of life cycles, meiosis, and sexual reproduction with an emphasis on plants, which are here broadly defined to include the polyphyletic algae and the monophyletic land plants [9–12]. We will provide evidence that all algal and land plant life cycles are variations of one basic theme, and differ only in the extent to which multicellularity is expressed in the haploid or diploid phase. We also argue that an often underappreciated selective advantage of multicellularity is that it increases fecundity. We also revive the possibility that meiosis evolved first as a mechanism to deal with auto-polyploidy, as originally suggested by Cleveland [13] and independently proposed by others [14–16]. Finally, we present a scenario for the evolution of the alternation of generations and the ascendency of the diploid phase during land plant evolution. We focus, albeit not exclusively, on the algae and the land plants for five reasons: (1) their phyletic relationships are well established, (2) their biotic diversity equals or exceeds that of any other group of eukaryotes, (3) the algae are polyphyletic and thus provide insights into convergent evolution, (4) the
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Did meiosis evolve before sex and the evolution of eukaryotic life cycles?
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Figure 1. A: The life cycle of a mammal (Rattus) and B: the life cycle of a heterosporous fern (Marsilia) showing one of the consequences of oocyte (egg) formation in the former and the absence of oocytes in the latter (1n ¼ haploid chromosome number; 2n ¼ diploid chromosome number). For simplicity, each multicellular diploid phase is depicted with a genome consisting of two alleles of a gene (ab). In this hypothetical case, the a allele is lost during the formation of the egg and the three polar bodies such that the F1 rat is homozygous bb. In contrast, the mega- and microsporophytes of the fern produce spores carrying the a allele and the b allele in equal numbers that in turn can potentially produce equal numbers of gametophytes carrying both alleles (original drawings).
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literature discussing life cycles and the evolution of meiosis is zoocentric, and (5) many aspects of plant reproduction differ significantly from that of animals or fungi in ways that challenge traditional models for the costs and benefits of meiosis. For example, among mammals every allele in a primary oocyte has a 50% chance of being eliminated in the polar bodies (Fig. 1A). Every allele therefore gains a two-fold selective advantage when meiosis is suppressed. Yet, within the life cycle of a species that has a unisexual (sperm- or eggproducing) gametophyte, the same allele has only a 33.3% chance of being eliminated because polar bodies do not form Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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land plant–like Figure 2. Schematics of life cycles of algae and plants (1n ¼ haploid chromosome number; 2n ¼ diploid chromosome number). A: The simplest life cycles consists of an alternation between a unicellular haploid phase and a unicellular diploid phase (Chlamydomonas). B: The expression of multicellularity in the haploid phase (Chara) or C: in the diploid phase (Fucus) results in a haplobiontic life cycle. D: The expression of multicellularity in both phases results in a diplobiontic life cycle characteristic of the embryophytes (Marsilia). E: The diploid phase can have two phenotypes, for example, the life cycle of late-divergent red algae (Polysiphonia) (see Fig. 3B) (original drawings).
(Fig. 1B). Likewise, among metazoans, males and females normally each contribute 50% of their genome to their progeny, whereas uniparental inheritance of chloroplast DNA in plants can be either paternal or maternal, depending on the lineage [17].
Eukaryotic life cycles are fundamentally the same The diversity of life cycles containing mechanisms for sexual reproduction and the ecological and evolutionary persistence of what have been described as exclusively asexual species have been described as two of the great dilemmas in evolutionary biology [4, 5]. If natural selection acts persistently and if meiosis and the fusion of gametes (syngamy) are fundamental attributes of sexual reproduction, why should so many different life histories exist, sometimes even in the same lineage? Further, if sexual reproduction is the primary source of variation in populations, as suggested by August Weismann Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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Polysiphonia–like (1834–1914), how can asexual species persist over extended ecological and evolutionary time? Indeed, many distinguished evolutionists have struggled to understand why sexual reproduction evolved in the first place [4–8, 18, 19]. These and other open-ended questions are particularly perplexing in light of the life cycles of the algae and the land plants that, unlike metazoans, manifest considerable variation [9–11, 20–22]. For example, some life cycles are dominated by the haploid phase (e.g. the green alga Spirogyra, the xanthophycean yellow-green alga Tribonema, and the mosses), whereas others are dominated by the diploid phase (e.g. vascular plants, Fig. 1B and the brown alga Fucus). In those that possess more than one multicellular phase, some life cycles are isomorphic (e.g. the green alga Ulva and the brown alga Ectocarpus), others are heteromorphic (e.g. the green alga Derbesia and the brown alga Laminaria), and still others are trimorphic (e.g. the red alga Polysiphonia). Yet, all of these variations are fundamentally the same. In addition to the capacity for asexual reproduction, each life cycle involves fusion of gametes (syngamy), meiosis, and an alternation between a haploid and a diploid unicellular or multicellular phase (Fig. 2), or their equivalent euploid levels in life cycles that normally involve endoduplication or that evolved as a result of auto-polyploidy. The primary difference among them lies in the duration of the haploid and diploid phase and in whether multicellularity is expressed in one or both of these phases. It is generally held that the ancestral life cycle in each algal clade involved an alternation between a unicellular haploid cell and a diploid cell (Fig. 2A), much like the life cycle of Chlamydomonas (Fig. 3A), and that either or both unicellular phases had the ability to replicate asexually by mitotic division [9–11, 14, 20–23]. This “default” life cycle presumably
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Figure 3. Examples of how intercalated mitotic divisions amplify the benefits of fertilization (gray areas in each schematic identify the diploid phase in each life cycle). A: In the unicellular green alga Chlamydomonas, meiosis produces the unicellular haploid phase, which has two different mating types ( and þ strains). When stressed, the haploid cell encysts and undergoes mitotic division, which increases the number of cells that can subsequently develop into asexual zoospores, or gametes that undergo syngamy to produce zygotes. B: In the latedivergent red alga Polysiphonia, the multicellular diploid phase has two morphologically distinct phenotypes (the carposporophyte and the tetrasporophyte). The carposporophyte develops from the zygote and resides on the female gametophyte. It produces diploid carpospores that develop into the free-living diploid multicellular tetrasporophyte that subsequently produces haploid spores that grow into free-living, isomorphic gametophytes (see Fig. 2E). A and B adapted from Raven et al. [24] (Figs. 15–41 and 15–35, respectively).
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Among its many benefits, multicellularity increases fecundity
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The appearance of multicellularity in at least 25 lineages [28] raises two important questions. How and why did multicellu-
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Figure 4. The number of a unicellular and a two-celled alga (see inserts) plotted over successive generations (assuming no mortality and no intercalated asexual reproductive events). The multicellular alga quickly outnumbers the unicellular alga revealing that simple multicellularity increases population reproductive capacity and thus fitness (see Fig. 3A) (original drawings).
larity evolve? Numerous hypothetical scenarios have been advanced to answer these questions. However, the traditional approach focuses on extant species in the freshwater volvocine green algae, which have been arranged in a unicellular ) colonial ) multicellular body-plan transformational series to model the evolution of multicellularity [29, 30]. According to this model, the modification of the unicellular ancestral cell wall into an extracellular matrix gave rise to simple colonial aggregates (e.g. Tetrabaena socialis), whereas the appearance of additional, more derived, traits is inferred to result in forms ranging from colonies with complex, asymmetric cell division, to multicellular organisms with full germ-soma division of labor such as Volvox carteri [30]. Multilevel selection theory identifies two evolutionary phases in this transformation series: (1) an alignment-offitness phase, which requires genetic similarity among adjoining cells, and (2) an export-of-fitness phase, which requires cellular interdependence and collaboration [31–34]. The factors driving these phases are more problematic, although it is clear that multicellularity provides a number of advantages in addition to increasing reproductive output (for a detailed review, see [35]). For example, the acquisition of a colonial body plan can reduce the risk of predation as a consequence of achieving larger sizes [36–38], which may explain the rapid divergent evolution of multicellularity occurring at 1,500 Mya after the evolution of phagocytosis [39]. The colonial body plan also allows different cells – via physiological specialization – to utilize different resources, even the in absence of morphological differentiation [28, 29, 35]. For example, undifferentiated colonies resulting from incomplete cell separation of Saccharomyces cerevisiae appear spontaneously in cultures with low sucrose concentrations [40]. The cells in these colonies cooperate in ways that reduce starvation and provide mutual protection. Holmes et al. [40] have shown that an ethanol-induced prion formed from the Mot3 transcription factor alters the expression of FLO11 (a major factor governing cell-cell adhesion in this species) and induces multicellularity. Oud et al. [41] have shown that genome duplication and ACE2 mutations can also induce multicellularity. Further, experiments using the coccolithophyte Phaeocystis show that the colonial phenotype has faster rates of cell division compared to the unicellular phenotype [42], perhaps because the extracellular adhesive matrix can be used to store nutrients that can be utilized under conditions of environmental stress. These and other advantages are perpetuated in multicellular body plans (reviewed in [35]). For example, the encapsulation of nuclei into separate but interconnected cells establishes discrete physiological boundaries that permit the isolation of different molecular regulators, trafficking routes, cytosolic recycling, transcytosis, exocytosis, and metabolite degradation. Intercellular communication within a multicellular organism also permits coordination among these processes to establish, maintain or switch supracellular physiological domains as well as a stratagem for segregating and isolating defective nuclei resulting from deleterious mutations [43], which are known to accumulate at cell- and tissue-specific rates [44]. However, in the context of this article, we draw particular attention to the fact that multicellularity increases fecundity by increasing the number of cells that can participate in
evolved during the Precambrian and was subsequently evolutionarily modified by the intercalation of mitotic divisions in one or both phases. For example, the appearance of multicellularity in the haploid phase resulting from mitotic divisions after zygotic meiosis yielded the life cycle of the freshwater charophycean algae Chara and Coleochaete (Fig. 2B), whereas the evolution of multicellularity in the diploid phase resulting from mitotic divisions before gametic meiosis produced the life cycle of the marine alga Fucus (Fig. 2C), and, by convergent evolution, typical metazoans such as mammals (Fig. 1A). Finally, the appearance of multicellularity in both the haploid and the diploid phase by means of delayed zygotic meiosis and sporic meiosis independently resulted in the life cycle of the green marine alga Ulva and the land plants (Fig. 2D). Variants of these three basic life cycles certainly exist. For example, the life cycles of some red algae, such as Polysiphonia, contain more than one diploid multicellular organism (Fig. 3B) and can involve curious and striking intraorganismic differences in the number of nuclei per cell and ploidy levels [25, 26]. The manifestation of multiple forms of the diploid phase confers a number of benefits, not least of which is an amplification of potentially rare fertilization events. For example, the gametes of red algae lack flagella [9–11], which can make fertilization events inefficient and even rare. The intercalation of two multicellular phases before zygotic meiosis occurs, and therefore may increase the number of gametophytes produced by any one zygote [14, 27]. A similar scheme is evident among some unicellular organisms (see Fig. 3A), which shows that there are alternative (albeit not as efficient) methods to increase fecundity in the absence of multicellularity.
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Figure 5. Scenarios for the evolution of meiosis and syngamy (pm ¼ plasma membrane, nm ¼ nuclear membrane); Scenario I (developed by John Maynard Smith [4]) and Scenario II (developed by Cleveland [13]). A–H: Two genetically different cells depicted with white and black chromosomes, (A) fuse to form a dikaryon with separate spindles (B and C) that becomes a diploid cell with a single spindle (D) with the capacity for chiasmata and meiosis I and meiosis II (E–G). Subsequent syngamy then results in a diploid cell (H). I–P: Meiosis evolved to correct for auto-polyploidy as the haploid phase (I) undergoes spontaneous whole-genome doubling (J) followed by gene divergence (K). Using the single ancestral spindle (L), the diploid evolves the capacity for chiasmata, meiosis I and II, and syngamy (M–P) as in Scenario I (original drawings).
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reproduction [27]. Inspection of the presumably ancestral eukaryotic life cycle (Fig. 2A) shows that two unicellular “adults” must take on the function of gametes, and thus are consumed in each cycle of sexual reproduction via syngamy, i.e. each cycle results in a net gain of only two individuals. In contrast, a haploid multicellular organism consisting of only two cells, one of which functions as a gamete, will quickly outcompete its unicellular counterpart (Fig. 4), even if it takes proportionally longer to reproduce. This competitive edge may explain why many organisms evolved delayed zygotic or gametic meiosis and intercalate mitotic divisions [20, 21] (see Fig. 3).
Meiosis was an adaptive response to auto-polyploidy Returning to the diversity of life cycles in the algae and land plants, we see that meiosis and syngamy occur in every
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variant (see Fig. 2). Yet, no model for the evolution of meiosis has been proposed without being criticized, sometimes even by its creators. For example, Maynard Smith [4] proposed perhaps the best known scenario for the evolution of meiosis and sexual reproduction in which two haploid cells fuse to produce a diploid heterokaryon with separate spindles (Fig. 5A–C Scenario I) that subsequently evolves into a diploid cell with one spindle, followed by the evolution of chiasmata, meiosis, and syngamy (Fig. 5D–H). However, although this model is plausible, Maynard Smith rejected it because it first asserts that organisms “… give up genetic variability for hybrid vigour; then abandon hybrid vigour for the benefits of variability; finally, regain hybrid vigour through reduction division and syngamy” [4]. We argue that a more parsimonious scenario emerges from a proposition made by Cleveland [13], i.e. meiosis evolved as a mechanism to correct for spontaneous whole-genome duplication (auto-polyploidy or endoduplication), an idea that was independently proposed by others [14–16]. This scenario Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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Figure 6. Proto-meiosis and the diversity of haploid unicellular protists (eukaryotic microorganisms). A–D: Redaction of Scenario II (see Fig. 5) in which meiosis evolves before syngamy, genomic divergence, and chiasmata. In this version, auto-polyploidy (A and B) is followed by a one-step early form of meiosis (C and D) that immediately reestablishes the ancestral euploid level (see arrow). E: Different early forms of proto-meiosis may explain why so many variants of meiosis exist since the evolutionary divergence of diverse unicellular eukaryotic lineages. From upper left to lower right: shell of an amoeboid protist (Foraminifera), a ciliate (Entodiniomorpha), an amoeba (Amoeba sp.), a flagellated protozoon (Trichomonas sp.), a colonial ciliate (Opercularia sp.), a radiolarian, a gregarine (Apicomplexan protozoon), and a thecamoeba (amoeboid protozoon) (original drawings).
removes the necessity of evolving syngamy before meiosis and the necessity of reducing dikaryontic spindles to one (Fig. 5I–L Scenario II), while permitting the subsequent sequence of events proposed by Maynard Smith (Fig. 5K–P). A more simplified scenario asserts that syngamy, genomic variation, and chiasmata evolved later (Fig. 6 A–D), perhaps in response to the problems arising from poly-valency, gene over-expression, aneuploidy, and other negative consequences of polyploidy [45]. This scenario, in which meiosis increases fecundity, (1) evades the negative aspects of the “cost” of segregational genetic load (i.e. the fitness cost of breaking down genetic correlations and linkage disequilibria established previously by natural selection), (2) avoids the need Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
to invoke multilevel selection theory to explain the evolution of meiosis (because the benefits of meiosis are conferred immediately during cell division), (3) is consistent with the existence of different recombination-independent mechanisms in homologous chromosome pairing [46, 47] (because the scenario predicts some form of “proto-meiosis” before ancient eukaryotes diversified into the current extant Kingdoms), and (4) is compatible with the prevalence of unicellular haploid (as opposed to unicellular diploid) species in diverse protists (Fig. 6E). As in the case of the Maynard Smith model, Cleveland’s proposition does not provide a mechanistic explanation for the evolution of the unique features of meiosis, e.g. homolog pairing, the suppression of centromere splitting, and the absence of the S phase. However, a variety of dinoflagellates, sporozoa, archaezoans, and parabasalia undergo one-step meiosis, that is, chromosome segregation occurs before duplication [48, 49]. This phenomenon indicates that the critical evolutionary innovation was the acquisition of mechanisms capable of juxtaposing homologs to form bivalents (i.e. synapse), and their concomitant separation [16]; this is likely, in particular, because the capacity for recombination occurs among prokaryotes and therefore predates meiosis [49, 50]. How this happened remains unknown, although research has shown that chromosomes that fail to undergo chromatin remodeling loose their competency to pair [51]. For example, chromatin reorganization in the leptotene-to-
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zygotene transition is required for normal chromosome dynamics in maize [52], whereas telomere and centromere interactions in early meiosis evoke chromatin conformational changes required for pairing interactions [53]. Nevertheless, the molecular mechanisms underlying meiotic chromatin reorganization and homolog pairing are unclear, and other factors are undoubtedly important.
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indicate that multicellularity most likely appeared first in the haploid generation (see Fig. 2B) and subsequently in the diploid generation within each of these three lineages [3, 12, 14, 22, 35, 55–58]. This parallel sequence of events raises a simple question: why did multicellularity evolve in the haploid phase first and in the diploid phase second?
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Sexual reproduction is maintained for different reasons So, what is the current adaptive value of meiosis followed by syngamy? Or more precisely, why is sexual reproduction retained in so many species? Many workers have attempted to provide a single canonical answer, but none has provided an explanation that has satisfied everyone. Our view is that (1) meiosis does more than just provide for additive genetic variation, e.g. the repair of double strand DNA damage, the maintenance of euploidy, resetting epigenetic mechanisms, and a method for purging deleterious genomes (see [14–16]), (2) natural selection has acted on each of its functionalities with different degrees of intensity over evolutionary time, and thus (3) different organisms currently maintain sexual reproduction for a variety of reasons. This perspective may not be satisfying to those who desire a single reason for the existence and maintenance of sex. However, the current available information is consistent with these three propositions. Although the evolution of apomictic species within very different lineages of plants, animals, and fungi attests, at the very least, to the shortterm gains of asexual reproduction, no known asexual variant has been observed to out-compete and displace its sexually reproducing conspecific, even in stable environments. This fact argues strongly for the ecological importance of sexual reproduction sensu The Tangled Bank hypothesis [8]. We also draw attention to an important immediate shortterm advantage of sexual reproduction – sex generates variation among siblings, which can reduce sibling competition (also known as sibling rivalry) [4–8, 35]. A sexually reproducing organism will have fewer surviving progeny if there is competition among siblings, and competition will likely increase as the genetic similarity of siblings increases [6, 8]. Meiosis and syngamy reduce the genetic similarity among progeny and thus reduce competition. The 50% cost of sex might be counterbalanced by an increased potential for progeny to survive. This might be the case in particular when the potential for dispersal is low (when “the apple doesn’t fall far from the tree”) [54].
Multicellularity appears first in the haploid phase Life cycles that have an alternation between a multicellular haploid and a multicellular diploid generation (see Fig. 2D) occur in the brown algae, the green algae, and the land plants. In each case, these life cycles are posited to have evolved from a life cycle similar to that of Chlamydomonas (see Figs. 2A and 3A). Comparative phenotypic and molecular studies also
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Whether multicellularity evolves in the haploid or diploid phase, or in both phases, depends on a number of factors including an organism’s population genetics [6–8] and its environmental context [20, 21, 35]. Here, we focus on the former, since the frequency of convergent evolution in the life cycles of marine and freshwater algae and in the land plants is very high. If the haploid phase is multicellular, its gametes will be genetically homogenous, and, if self-compatible, many of its progeny resulting from sexual reproduction will be clones [8]. Meiosis will recombine and resort the haploid genome after syngamy, but the fitness of a population of haploid multicellular organisms (with a Chlamydomonas-like life cycle) is nevertheless limited because all zygotes contain at least one-half of the haploid’s genome. In contrast, if the diploid is multicellular, its gametes will be genetically diverse as a result of gametic meiosis. Thus, an organism with zygotic meiosis will likely produce progeny with less genetic variance than the progeny produced by an organism with gametic meiosis [8]. The extent to which this holds true depends on other factors. For example, if genetic variation is predominantly maintained by selection acting on gene frequency, gametic meiosis will be more effective at maintaining genetic variation than zygotic meiosis. Likewise, as long as the expression of deleterious alleles is sufficiently masked by the wild-type allele in the heterozygous condition, genetic models show that diploidy is favored over haploidy [59]. However, when the rate of recombination is low, diploidy is much less likely to be favored over haploidy, regardless of environmental context [8]. In fact, according to one model, the evolution of diploidy is impossible without significant levels of recombination, even when the masking of deleterious alleles is strong [60].
Meiotic drive Consider the consequences of selection acting primarily on gamete function with or without its effect on diploid fitness, a phenomenon called meiotic drive [61, 62]. In life cycles with only a multicellular diploid phase (such as Fucus), the alleles for gamete function will segregate during meiosis to subsequently create a population of diploids that can maintain these alleles under constant selection for alleles that enhance gamete-function. In contrast, zygotic meiosis (and the Chlamydomonas-like life cycle) will result in haploids containing alleles that are either less or more fit for gamete function, such that multicellular individuals bearing the less fit alleles will be at a disadvantage, thereby reducing the effective population size of reproductively viable individuals. The effect of gametic meiosis on the genetic Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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The heterozyote advantage An explanation for the shift from a diplobiontic life cycle dominated by the haploid phase to one dominated by the diploid phase observed during land plant evolution requires more elaboration (for a detailed review, see [35]), because simple genetic models show that heterozygote advantage can lead to an increase in the dominance of the diploid phase, but only if the diploid phase is already sufficiently dominant [63]. The requirement for diploid dominance is inconsistent with our current understanding of green algal and the land plant evolution, which indicates that the ancestral condition was unicellular and haploid [12, 58]. Genetic models also show that doubling the rate of mutation by means of diploidy has the potential to actually slow adaptive evolution in both asexually and sexually reproducing organisms ([60]; see also [15, 18]). The most frequently proposed explanation for the final dominance of the diploid phase is heterozygote advantage [35, 64–66], i.e. where the heterozygote genome has a higher relative fitness than the homozygote dominant or recessive genome. Heterozygotes can carry a “silenced” mutational load that is free to mutate in ways that can become beneficial [67– 69]. The diploid condition can be particularly beneficial in large, multicellular organisms, which can carry recessive somatic mutations [70]. However, diploids do not invariably have an advantage, and the recessive somatic mutation hypothesis does not explain why multicellularity evolved in the diploid phase. Consider a hypothetical gene with a bellshaped expression level pattern with an optimum at 1.0 and a haploid expression level of 0.5. Under these circumstances, the wild-type haploid phase is disadvantaged, because its expression level equals 0.5, whereas the wild-type homozygous phase has an optimum gene expression level of 1.0. Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
Consider now the effects of a mutation that doubles the expression level such that the haploid mutant has the optimal expression level of 1.0, whereas the mutant diploid has a suboptimal overexpression level of 1.5. In this scenario, the wild-type homozygous diploid (and the mutated haploid) has the advantage over the mutated heterozygous diploid, provided that mechanisms for non-DNA-sequence modification are unavailable. This scenario is clearly contrived, because it rests on a single gene and the opposite effects can be simulated if a mutation confers a slight advantage [65]. It is presented merely as a hypothetical example of heterozygote disadvantage, and not as a blanket denial of the benefits conferred by being a heterozygous diploid [64]. However, changes in gene expression are an important and prevalent mechanism for adaptation [71] and it is not uncommon for mutations of small effect to be adaptive when they modify expression levels, regardless of whether an organism is haploid or diploid.
Conclusions Although the homology of the life cycles of plants (here broadly defined to include the algae) was elucidated by 19th-century botanists (Wilhelm Hofmeister, Eduard Strasburger) [2, 3] and the germ line/soma-concept of animal development was outlined by August Weismann [8], the evolutionary interrelationships between these modes of reproduction remain enigmatic. Here, we have reviewed evidence that supports four propositions: (1) the fundamental difference among eukaryotic life cycles is whether multicellularity is expressed in the haploid or the diploid phase, or in both, (2) the evolution of multicellularity increases lifetime reproductive success (fitness) by increasing fecundity, (3) some early form of meiosis may have emerged as an adaptation to correct for the negative consequences of auto-polyploidy, and (4) it may have evolved before sexual reproduction sensu stricto (i.e. gamete fusion and the creation of a diploid zygote). We have also reviewed evidence that the reduction in sibling competition, which occurs in animals as well as plants, is an important driver for the retention of sexual reproduction in phylogenetically divergent eukaryotic lineages [72–75]. Some of this evidence is admittedly problematic, and much is incomplete. Future research toward understanding the homologies and analogies among the components of mitotic and meiotic cell cycles across diverse clades is required (and we hope will be forthcoming) to permit better-educated inferences about the evolutionary history of meiosis. This information will perhaps shed light on the sequence in which the unique features of meiosis evolved in diverse lines of animals, plants, and protists (Figs. 1A, B and 6E).
Acknowledgments This paper is dedicated to Prof. John Maynard Smith (1920– 2004) whose brilliance continues to stimulate and encourage generations of scholars. We thank the editor, the referees, and Dr. Yin-Long Qiu (University of Michigan) for their constructive and insightful comments. Support from the Alexander von Humboldt Foundation (Bonn, Germany) (AvH-Fellowship
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variance of alleles affecting gamete function will also depend on the intensity of competition among gametes. If competition is intense among gametes, only those gametes bearing superior alleles for gamete function will succeed at producing zygotes, such that multicellular diploids with gametic meiosis will have an advantage over their haploid counterparts. If, however, competition among gametes is low, the majority of gametes will be successful at forming zygotes such that multicellular haploids with zygotic meiosis will have the advantage [8]; this may explain the parallel evolution of zygotic meiosis in so many algal lineages. Achieving an alternation of generations likely did not require extensive genomic reorganization, since almost all unicellular eukaryotes are capable of asexual reproduction. Nevertheless, post-fertilization mitosis necessitated modifications in the onset of the cell cycle. If the ancestral haploid was multicellular, the expression of multicellularity in the diploid phase arguably presented no great challenge because the genomic potential for multicellularity already existed [22, 35]. Two reasonable deductions, therefore, are (1) the ancestral diplobiontic life cycle was isomorphic (as in the green alga Ulva) and (2) the evolution of a dimorphic life cycle had to confer some advantage, e.g. niche-partitioning as a countermeasure perhaps against predation.
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2012 to U. K., Stanford, California, USA) and the College of Agriculture and Life Sciences, Cornell University (to K. J. N.) is gratefully acknowledged.
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Karl J. Niklas1), Edward D. Cobb1) and Ulrich Kutschera2) Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for spontaneous whole-genome duplication (autopolyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition.
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Keywords: algae; alternation of generations; auto-polyploidy; chiasmata; embryophytes; meiosis; syngamy
Introduction In his Systema Naturae, Carl Linnaeus (1707–1778) placed all plants with hidden reproductive organs into a class he called “Cryptogamae” [1], a group that included fungi, lichens,
DOI 10.1002/bies.201400045 1)
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Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA Institute of Biology, University of Kassel, Kassel, Germany
*Corresponding author: Karl J. Niklas E-mail: [email protected]
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algae, bryophytes, and pteridophytes. Although the German bryologist Johannes Hedwig (1730–1799) had discovered structures he attributed to sexual reproduction, the life cycle of early-divergent land plants (e.g. mosses and ferns) remained enigmatic until the publication of a remarkable monograph written by Wilhelm Hofmeister (1824–1877), who summarized his discoveries during the 1840s concerning the modes of reproduction of cryptogams [2]. In this monograph, Hofmeister concluded that the land plant life cycles had an alternation of two generations in which germinating spores develop into plants bearing sperm-producing antheridia and egg-producing archegonia (the gametophyte). After fertilization by sperm, the gametophytes produce plants that develop into a second multicellular generation (the sporophyte) that ultimately gives rise to the next generation of spores [2]. Thus, Hofmeister asserted the homology of land plant gametophytes and sporophytes. Over 40 years later, Eduard Strasburger (1844–1912) proposed that the land plant life cycle involved an alternation between a haploid gametophytic phase and a diploid sporophytic phase [3]. Despite these early insights, much of the evolution of the life cycles and reproduction remains unknown or problematic [4–8]. Here, we explore these topics in the hope of providing an additional perspective on the evolution of life cycles, meiosis, and sexual reproduction with an emphasis on plants, which are here broadly defined to include the polyphyletic algae and the monophyletic land plants [9–12]. We will provide evidence that all algal and land plant life cycles are variations of one basic theme, and differ only in the extent to which multicellularity is expressed in the haploid or diploid phase. We also argue that an often underappreciated selective advantage of multicellularity is that it increases fecundity. We also revive the possibility that meiosis evolved first as a mechanism to deal with auto-polyploidy, as originally suggested by Cleveland [13] and independently proposed by others [14–16]. Finally, we present a scenario for the evolution of the alternation of generations and the ascendency of the diploid phase during land plant evolution. We focus, albeit not exclusively, on the algae and the land plants for five reasons: (1) their phyletic relationships are well established, (2) their biotic diversity equals or exceeds that of any other group of eukaryotes, (3) the algae are polyphyletic and thus provide insights into convergent evolution, (4) the
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literature discussing life cycles and the evolution of meiosis is zoocentric, and (5) many aspects of plant reproduction differ significantly from that of animals or fungi in ways that challenge traditional models for the costs and benefits of meiosis. For example, among mammals every allele in a primary oocyte has a 50% chance of being eliminated in the polar bodies (Fig. 1A). Every allele therefore gains a two-fold selective advantage when meiosis is suppressed. Yet, within the life cycle of a species that has a unisexual (sperm- or eggproducing) gametophyte, the same allele has only a 33.3% chance of being eliminated because polar bodies do not form Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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(Fig. 1B). Likewise, among metazoans, males and females normally each contribute 50% of their genome to their progeny, whereas uniparental inheritance of chloroplast DNA in plants can be either paternal or maternal, depending on the lineage [17].
Eukaryotic life cycles are fundamentally the same The diversity of life cycles containing mechanisms for sexual reproduction and the ecological and evolutionary persistence of what have been described as exclusively asexual species have been described as two of the great dilemmas in evolutionary biology [4, 5]. If natural selection acts persistently and if meiosis and the fusion of gametes (syngamy) are fundamental attributes of sexual reproduction, why should so many different life histories exist, sometimes even in the same lineage? Further, if sexual reproduction is the primary source of variation in populations, as suggested by August Weismann Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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Polysiphonia–like (1834–1914), how can asexual species persist over extended ecological and evolutionary time? Indeed, many distinguished evolutionists have struggled to understand why sexual reproduction evolved in the first place [4–8, 18, 19]. These and other open-ended questions are particularly perplexing in light of the life cycles of the algae and the land plants that, unlike metazoans, manifest considerable variation [9–11, 20–22]. For example, some life cycles are dominated by the haploid phase (e.g. the green alga Spirogyra, the xanthophycean yellow-green alga Tribonema, and the mosses), whereas others are dominated by the diploid phase (e.g. vascular plants, Fig. 1B and the brown alga Fucus). In those that possess more than one multicellular phase, some life cycles are isomorphic (e.g. the green alga Ulva and the brown alga Ectocarpus), others are heteromorphic (e.g. the green alga Derbesia and the brown alga Laminaria), and still others are trimorphic (e.g. the red alga Polysiphonia). Yet, all of these variations are fundamentally the same. In addition to the capacity for asexual reproduction, each life cycle involves fusion of gametes (syngamy), meiosis, and an alternation between a haploid and a diploid unicellular or multicellular phase (Fig. 2), or their equivalent euploid levels in life cycles that normally involve endoduplication or that evolved as a result of auto-polyploidy. The primary difference among them lies in the duration of the haploid and diploid phase and in whether multicellularity is expressed in one or both of these phases. It is generally held that the ancestral life cycle in each algal clade involved an alternation between a unicellular haploid cell and a diploid cell (Fig. 2A), much like the life cycle of Chlamydomonas (Fig. 3A), and that either or both unicellular phases had the ability to replicate asexually by mitotic division [9–11, 14, 20–23]. This “default” life cycle presumably
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Figure 3. Examples of how intercalated mitotic divisions amplify the benefits of fertilization (gray areas in each schematic identify the diploid phase in each life cycle). A: In the unicellular green alga Chlamydomonas, meiosis produces the unicellular haploid phase, which has two different mating types ( and þ strains). When stressed, the haploid cell encysts and undergoes mitotic division, which increases the number of cells that can subsequently develop into asexual zoospores, or gametes that undergo syngamy to produce zygotes. B: In the latedivergent red alga Polysiphonia, the multicellular diploid phase has two morphologically distinct phenotypes (the carposporophyte and the tetrasporophyte). The carposporophyte develops from the zygote and resides on the female gametophyte. It produces diploid carpospores that develop into the free-living diploid multicellular tetrasporophyte that subsequently produces haploid spores that grow into free-living, isomorphic gametophytes (see Fig. 2E). A and B adapted from Raven et al. [24] (Figs. 15–41 and 15–35, respectively).
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Figure 4. The number of a unicellular and a two-celled alga (see inserts) plotted over successive generations (assuming no mortality and no intercalated asexual reproductive events). The multicellular alga quickly outnumbers the unicellular alga revealing that simple multicellularity increases population reproductive capacity and thus fitness (see Fig. 3A) (original drawings).
larity evolve? Numerous hypothetical scenarios have been advanced to answer these questions. However, the traditional approach focuses on extant species in the freshwater volvocine green algae, which have been arranged in a unicellular ) colonial ) multicellular body-plan transformational series to model the evolution of multicellularity [29, 30]. According to this model, the modification of the unicellular ancestral cell wall into an extracellular matrix gave rise to simple colonial aggregates (e.g. Tetrabaena socialis), whereas the appearance of additional, more derived, traits is inferred to result in forms ranging from colonies with complex, asymmetric cell division, to multicellular organisms with full germ-soma division of labor such as Volvox carteri [30]. Multilevel selection theory identifies two evolutionary phases in this transformation series: (1) an alignment-offitness phase, which requires genetic similarity among adjoining cells, and (2) an export-of-fitness phase, which requires cellular interdependence and collaboration [31–34]. The factors driving these phases are more problematic, although it is clear that multicellularity provides a number of advantages in addition to increasing reproductive output (for a detailed review, see [35]). For example, the acquisition of a colonial body plan can reduce the risk of predation as a consequence of achieving larger sizes [36–38], which may explain the rapid divergent evolution of multicellularity occurring at 1,500 Mya after the evolution of phagocytosis [39]. The colonial body plan also allows different cells – via physiological specialization – to utilize different resources, even the in absence of morphological differentiation [28, 29, 35]. For example, undifferentiated colonies resulting from incomplete cell separation of Saccharomyces cerevisiae appear spontaneously in cultures with low sucrose concentrations [40]. The cells in these colonies cooperate in ways that reduce starvation and provide mutual protection. Holmes et al. [40] have shown that an ethanol-induced prion formed from the Mot3 transcription factor alters the expression of FLO11 (a major factor governing cell-cell adhesion in this species) and induces multicellularity. Oud et al. [41] have shown that genome duplication and ACE2 mutations can also induce multicellularity. Further, experiments using the coccolithophyte Phaeocystis show that the colonial phenotype has faster rates of cell division compared to the unicellular phenotype [42], perhaps because the extracellular adhesive matrix can be used to store nutrients that can be utilized under conditions of environmental stress. These and other advantages are perpetuated in multicellular body plans (reviewed in [35]). For example, the encapsulation of nuclei into separate but interconnected cells establishes discrete physiological boundaries that permit the isolation of different molecular regulators, trafficking routes, cytosolic recycling, transcytosis, exocytosis, and metabolite degradation. Intercellular communication within a multicellular organism also permits coordination among these processes to establish, maintain or switch supracellular physiological domains as well as a stratagem for segregating and isolating defective nuclei resulting from deleterious mutations [43], which are known to accumulate at cell- and tissue-specific rates [44]. However, in the context of this article, we draw particular attention to the fact that multicellularity increases fecundity by increasing the number of cells that can participate in
evolved during the Precambrian and was subsequently evolutionarily modified by the intercalation of mitotic divisions in one or both phases. For example, the appearance of multicellularity in the haploid phase resulting from mitotic divisions after zygotic meiosis yielded the life cycle of the freshwater charophycean algae Chara and Coleochaete (Fig. 2B), whereas the evolution of multicellularity in the diploid phase resulting from mitotic divisions before gametic meiosis produced the life cycle of the marine alga Fucus (Fig. 2C), and, by convergent evolution, typical metazoans such as mammals (Fig. 1A). Finally, the appearance of multicellularity in both the haploid and the diploid phase by means of delayed zygotic meiosis and sporic meiosis independently resulted in the life cycle of the green marine alga Ulva and the land plants (Fig. 2D). Variants of these three basic life cycles certainly exist. For example, the life cycles of some red algae, such as Polysiphonia, contain more than one diploid multicellular organism (Fig. 3B) and can involve curious and striking intraorganismic differences in the number of nuclei per cell and ploidy levels [25, 26]. The manifestation of multiple forms of the diploid phase confers a number of benefits, not least of which is an amplification of potentially rare fertilization events. For example, the gametes of red algae lack flagella [9–11], which can make fertilization events inefficient and even rare. The intercalation of two multicellular phases before zygotic meiosis occurs, and therefore may increase the number of gametophytes produced by any one zygote [14, 27]. A similar scheme is evident among some unicellular organisms (see Fig. 3A), which shows that there are alternative (albeit not as efficient) methods to increase fecundity in the absence of multicellularity.
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Figure 5. Scenarios for the evolution of meiosis and syngamy (pm ¼ plasma membrane, nm ¼ nuclear membrane); Scenario I (developed by John Maynard Smith [4]) and Scenario II (developed by Cleveland [13]). A–H: Two genetically different cells depicted with white and black chromosomes, (A) fuse to form a dikaryon with separate spindles (B and C) that becomes a diploid cell with a single spindle (D) with the capacity for chiasmata and meiosis I and meiosis II (E–G). Subsequent syngamy then results in a diploid cell (H). I–P: Meiosis evolved to correct for auto-polyploidy as the haploid phase (I) undergoes spontaneous whole-genome doubling (J) followed by gene divergence (K). Using the single ancestral spindle (L), the diploid evolves the capacity for chiasmata, meiosis I and II, and syngamy (M–P) as in Scenario I (original drawings).
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reproduction [27]. Inspection of the presumably ancestral eukaryotic life cycle (Fig. 2A) shows that two unicellular “adults” must take on the function of gametes, and thus are consumed in each cycle of sexual reproduction via syngamy, i.e. each cycle results in a net gain of only two individuals. In contrast, a haploid multicellular organism consisting of only two cells, one of which functions as a gamete, will quickly outcompete its unicellular counterpart (Fig. 4), even if it takes proportionally longer to reproduce. This competitive edge may explain why many organisms evolved delayed zygotic or gametic meiosis and intercalate mitotic divisions [20, 21] (see Fig. 3).
Meiosis was an adaptive response to auto-polyploidy Returning to the diversity of life cycles in the algae and land plants, we see that meiosis and syngamy occur in every
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variant (see Fig. 2). Yet, no model for the evolution of meiosis has been proposed without being criticized, sometimes even by its creators. For example, Maynard Smith [4] proposed perhaps the best known scenario for the evolution of meiosis and sexual reproduction in which two haploid cells fuse to produce a diploid heterokaryon with separate spindles (Fig. 5A–C Scenario I) that subsequently evolves into a diploid cell with one spindle, followed by the evolution of chiasmata, meiosis, and syngamy (Fig. 5D–H). However, although this model is plausible, Maynard Smith rejected it because it first asserts that organisms “… give up genetic variability for hybrid vigour; then abandon hybrid vigour for the benefits of variability; finally, regain hybrid vigour through reduction division and syngamy” [4]. We argue that a more parsimonious scenario emerges from a proposition made by Cleveland [13], i.e. meiosis evolved as a mechanism to correct for spontaneous whole-genome duplication (auto-polyploidy or endoduplication), an idea that was independently proposed by others [14–16]. This scenario Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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Figure 6. Proto-meiosis and the diversity of haploid unicellular protists (eukaryotic microorganisms). A–D: Redaction of Scenario II (see Fig. 5) in which meiosis evolves before syngamy, genomic divergence, and chiasmata. In this version, auto-polyploidy (A and B) is followed by a one-step early form of meiosis (C and D) that immediately reestablishes the ancestral euploid level (see arrow). E: Different early forms of proto-meiosis may explain why so many variants of meiosis exist since the evolutionary divergence of diverse unicellular eukaryotic lineages. From upper left to lower right: shell of an amoeboid protist (Foraminifera), a ciliate (Entodiniomorpha), an amoeba (Amoeba sp.), a flagellated protozoon (Trichomonas sp.), a colonial ciliate (Opercularia sp.), a radiolarian, a gregarine (Apicomplexan protozoon), and a thecamoeba (amoeboid protozoon) (original drawings).
removes the necessity of evolving syngamy before meiosis and the necessity of reducing dikaryontic spindles to one (Fig. 5I–L Scenario II), while permitting the subsequent sequence of events proposed by Maynard Smith (Fig. 5K–P). A more simplified scenario asserts that syngamy, genomic variation, and chiasmata evolved later (Fig. 6 A–D), perhaps in response to the problems arising from poly-valency, gene over-expression, aneuploidy, and other negative consequences of polyploidy [45]. This scenario, in which meiosis increases fecundity, (1) evades the negative aspects of the “cost” of segregational genetic load (i.e. the fitness cost of breaking down genetic correlations and linkage disequilibria established previously by natural selection), (2) avoids the need Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
to invoke multilevel selection theory to explain the evolution of meiosis (because the benefits of meiosis are conferred immediately during cell division), (3) is consistent with the existence of different recombination-independent mechanisms in homologous chromosome pairing [46, 47] (because the scenario predicts some form of “proto-meiosis” before ancient eukaryotes diversified into the current extant Kingdoms), and (4) is compatible with the prevalence of unicellular haploid (as opposed to unicellular diploid) species in diverse protists (Fig. 6E). As in the case of the Maynard Smith model, Cleveland’s proposition does not provide a mechanistic explanation for the evolution of the unique features of meiosis, e.g. homolog pairing, the suppression of centromere splitting, and the absence of the S phase. However, a variety of dinoflagellates, sporozoa, archaezoans, and parabasalia undergo one-step meiosis, that is, chromosome segregation occurs before duplication [48, 49]. This phenomenon indicates that the critical evolutionary innovation was the acquisition of mechanisms capable of juxtaposing homologs to form bivalents (i.e. synapse), and their concomitant separation [16]; this is likely, in particular, because the capacity for recombination occurs among prokaryotes and therefore predates meiosis [49, 50]. How this happened remains unknown, although research has shown that chromosomes that fail to undergo chromatin remodeling loose their competency to pair [51]. For example, chromatin reorganization in the leptotene-to-
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zygotene transition is required for normal chromosome dynamics in maize [52], whereas telomere and centromere interactions in early meiosis evoke chromatin conformational changes required for pairing interactions [53]. Nevertheless, the molecular mechanisms underlying meiotic chromatin reorganization and homolog pairing are unclear, and other factors are undoubtedly important.
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indicate that multicellularity most likely appeared first in the haploid generation (see Fig. 2B) and subsequently in the diploid generation within each of these three lineages [3, 12, 14, 22, 35, 55–58]. This parallel sequence of events raises a simple question: why did multicellularity evolve in the haploid phase first and in the diploid phase second?
Population genetics
Sexual reproduction is maintained for different reasons So, what is the current adaptive value of meiosis followed by syngamy? Or more precisely, why is sexual reproduction retained in so many species? Many workers have attempted to provide a single canonical answer, but none has provided an explanation that has satisfied everyone. Our view is that (1) meiosis does more than just provide for additive genetic variation, e.g. the repair of double strand DNA damage, the maintenance of euploidy, resetting epigenetic mechanisms, and a method for purging deleterious genomes (see [14–16]), (2) natural selection has acted on each of its functionalities with different degrees of intensity over evolutionary time, and thus (3) different organisms currently maintain sexual reproduction for a variety of reasons. This perspective may not be satisfying to those who desire a single reason for the existence and maintenance of sex. However, the current available information is consistent with these three propositions. Although the evolution of apomictic species within very different lineages of plants, animals, and fungi attests, at the very least, to the shortterm gains of asexual reproduction, no known asexual variant has been observed to out-compete and displace its sexually reproducing conspecific, even in stable environments. This fact argues strongly for the ecological importance of sexual reproduction sensu The Tangled Bank hypothesis [8]. We also draw attention to an important immediate shortterm advantage of sexual reproduction – sex generates variation among siblings, which can reduce sibling competition (also known as sibling rivalry) [4–8, 35]. A sexually reproducing organism will have fewer surviving progeny if there is competition among siblings, and competition will likely increase as the genetic similarity of siblings increases [6, 8]. Meiosis and syngamy reduce the genetic similarity among progeny and thus reduce competition. The 50% cost of sex might be counterbalanced by an increased potential for progeny to survive. This might be the case in particular when the potential for dispersal is low (when “the apple doesn’t fall far from the tree”) [54].
Multicellularity appears first in the haploid phase Life cycles that have an alternation between a multicellular haploid and a multicellular diploid generation (see Fig. 2D) occur in the brown algae, the green algae, and the land plants. In each case, these life cycles are posited to have evolved from a life cycle similar to that of Chlamydomonas (see Figs. 2A and 3A). Comparative phenotypic and molecular studies also
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Whether multicellularity evolves in the haploid or diploid phase, or in both phases, depends on a number of factors including an organism’s population genetics [6–8] and its environmental context [20, 21, 35]. Here, we focus on the former, since the frequency of convergent evolution in the life cycles of marine and freshwater algae and in the land plants is very high. If the haploid phase is multicellular, its gametes will be genetically homogenous, and, if self-compatible, many of its progeny resulting from sexual reproduction will be clones [8]. Meiosis will recombine and resort the haploid genome after syngamy, but the fitness of a population of haploid multicellular organisms (with a Chlamydomonas-like life cycle) is nevertheless limited because all zygotes contain at least one-half of the haploid’s genome. In contrast, if the diploid is multicellular, its gametes will be genetically diverse as a result of gametic meiosis. Thus, an organism with zygotic meiosis will likely produce progeny with less genetic variance than the progeny produced by an organism with gametic meiosis [8]. The extent to which this holds true depends on other factors. For example, if genetic variation is predominantly maintained by selection acting on gene frequency, gametic meiosis will be more effective at maintaining genetic variation than zygotic meiosis. Likewise, as long as the expression of deleterious alleles is sufficiently masked by the wild-type allele in the heterozygous condition, genetic models show that diploidy is favored over haploidy [59]. However, when the rate of recombination is low, diploidy is much less likely to be favored over haploidy, regardless of environmental context [8]. In fact, according to one model, the evolution of diploidy is impossible without significant levels of recombination, even when the masking of deleterious alleles is strong [60].
Meiotic drive Consider the consequences of selection acting primarily on gamete function with or without its effect on diploid fitness, a phenomenon called meiotic drive [61, 62]. In life cycles with only a multicellular diploid phase (such as Fucus), the alleles for gamete function will segregate during meiosis to subsequently create a population of diploids that can maintain these alleles under constant selection for alleles that enhance gamete-function. In contrast, zygotic meiosis (and the Chlamydomonas-like life cycle) will result in haploids containing alleles that are either less or more fit for gamete function, such that multicellular individuals bearing the less fit alleles will be at a disadvantage, thereby reducing the effective population size of reproductively viable individuals. The effect of gametic meiosis on the genetic Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
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The heterozyote advantage An explanation for the shift from a diplobiontic life cycle dominated by the haploid phase to one dominated by the diploid phase observed during land plant evolution requires more elaboration (for a detailed review, see [35]), because simple genetic models show that heterozygote advantage can lead to an increase in the dominance of the diploid phase, but only if the diploid phase is already sufficiently dominant [63]. The requirement for diploid dominance is inconsistent with our current understanding of green algal and the land plant evolution, which indicates that the ancestral condition was unicellular and haploid [12, 58]. Genetic models also show that doubling the rate of mutation by means of diploidy has the potential to actually slow adaptive evolution in both asexually and sexually reproducing organisms ([60]; see also [15, 18]). The most frequently proposed explanation for the final dominance of the diploid phase is heterozygote advantage [35, 64–66], i.e. where the heterozygote genome has a higher relative fitness than the homozygote dominant or recessive genome. Heterozygotes can carry a “silenced” mutational load that is free to mutate in ways that can become beneficial [67– 69]. The diploid condition can be particularly beneficial in large, multicellular organisms, which can carry recessive somatic mutations [70]. However, diploids do not invariably have an advantage, and the recessive somatic mutation hypothesis does not explain why multicellularity evolved in the diploid phase. Consider a hypothetical gene with a bellshaped expression level pattern with an optimum at 1.0 and a haploid expression level of 0.5. Under these circumstances, the wild-type haploid phase is disadvantaged, because its expression level equals 0.5, whereas the wild-type homozygous phase has an optimum gene expression level of 1.0. Bioessays 36: 1091–1101, ß 2014 WILEY Periodicals, Inc.
Consider now the effects of a mutation that doubles the expression level such that the haploid mutant has the optimal expression level of 1.0, whereas the mutant diploid has a suboptimal overexpression level of 1.5. In this scenario, the wild-type homozygous diploid (and the mutated haploid) has the advantage over the mutated heterozygous diploid, provided that mechanisms for non-DNA-sequence modification are unavailable. This scenario is clearly contrived, because it rests on a single gene and the opposite effects can be simulated if a mutation confers a slight advantage [65]. It is presented merely as a hypothetical example of heterozygote disadvantage, and not as a blanket denial of the benefits conferred by being a heterozygous diploid [64]. However, changes in gene expression are an important and prevalent mechanism for adaptation [71] and it is not uncommon for mutations of small effect to be adaptive when they modify expression levels, regardless of whether an organism is haploid or diploid.
Conclusions Although the homology of the life cycles of plants (here broadly defined to include the algae) was elucidated by 19th-century botanists (Wilhelm Hofmeister, Eduard Strasburger) [2, 3] and the germ line/soma-concept of animal development was outlined by August Weismann [8], the evolutionary interrelationships between these modes of reproduction remain enigmatic. Here, we have reviewed evidence that supports four propositions: (1) the fundamental difference among eukaryotic life cycles is whether multicellularity is expressed in the haploid or the diploid phase, or in both, (2) the evolution of multicellularity increases lifetime reproductive success (fitness) by increasing fecundity, (3) some early form of meiosis may have emerged as an adaptation to correct for the negative consequences of auto-polyploidy, and (4) it may have evolved before sexual reproduction sensu stricto (i.e. gamete fusion and the creation of a diploid zygote). We have also reviewed evidence that the reduction in sibling competition, which occurs in animals as well as plants, is an important driver for the retention of sexual reproduction in phylogenetically divergent eukaryotic lineages [72–75]. Some of this evidence is admittedly problematic, and much is incomplete. Future research toward understanding the homologies and analogies among the components of mitotic and meiotic cell cycles across diverse clades is required (and we hope will be forthcoming) to permit better-educated inferences about the evolutionary history of meiosis. This information will perhaps shed light on the sequence in which the unique features of meiosis evolved in diverse lines of animals, plants, and protists (Figs. 1A, B and 6E).
Acknowledgments This paper is dedicated to Prof. John Maynard Smith (1920– 2004) whose brilliance continues to stimulate and encourage generations of scholars. We thank the editor, the referees, and Dr. Yin-Long Qiu (University of Michigan) for their constructive and insightful comments. Support from the Alexander von Humboldt Foundation (Bonn, Germany) (AvH-Fellowship
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variance of alleles affecting gamete function will also depend on the intensity of competition among gametes. If competition is intense among gametes, only those gametes bearing superior alleles for gamete function will succeed at producing zygotes, such that multicellular diploids with gametic meiosis will have an advantage over their haploid counterparts. If, however, competition among gametes is low, the majority of gametes will be successful at forming zygotes such that multicellular haploids with zygotic meiosis will have the advantage [8]; this may explain the parallel evolution of zygotic meiosis in so many algal lineages. Achieving an alternation of generations likely did not require extensive genomic reorganization, since almost all unicellular eukaryotes are capable of asexual reproduction. Nevertheless, post-fertilization mitosis necessitated modifications in the onset of the cell cycle. If the ancestral haploid was multicellular, the expression of multicellularity in the diploid phase arguably presented no great challenge because the genomic potential for multicellularity already existed [22, 35]. Two reasonable deductions, therefore, are (1) the ancestral diplobiontic life cycle was isomorphic (as in the green alga Ulva) and (2) the evolution of a dimorphic life cycle had to confer some advantage, e.g. niche-partitioning as a countermeasure perhaps against predation.
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2012 to U. K., Stanford, California, USA) and the College of Agriculture and Life Sciences, Cornell University (to K. J. N.) is gratefully acknowledged.
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