Molecular Biology of the Cell - Volume 3 - Alberts B., Bray D., Lewis J., Raff M., Roberts K., Watson J. 1994

From Cells to Multicellular Organisms
Germ Cells and Fertilization
Advantages of Sexual Reproduction

Sexual reproduction involves the alternation of haploid Cell generations, each possessing a single set of Chromosomes, with diploid generations, where Cells carry a double set (Fig. 15-2). Genome mixing occurs through the fusion of two haploid cells to form a single diploid cell. In turn, new haploid cells are generated from diploid ones via a specialized type of division called Meiosis. During genetic recombination in meiosis, homologous chromosomes exchange DNA segments, after which these novel combinations segregate into separate cells that now contain single chromosome sets (see Section 15.2.2). As a result, each cell of the new haploid generation receives a fresh combination of genes derived partly from one parent of the preceding haploid generation and partly from the other. Thus, through cycles encompassing the haploid phase, gamete fusion, the diploid phase, and meiosis, old Gene combinations are broken up and new ones are created.

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Fig. 15-1. A Hydra budding off two new offspring (indicated by arrows). The descendants are genetically identical to the parent Organism; eventually, they detach and begin an independent existence. (Courtesy of Matai Hornbruch.)

15.1.1. In Multicellular animals, the diploid phase is complex and prolonged, whereas the haploid phase is simple and brief

During the sexual cycle, cells proliferate through standard mitotic division—most commonly during the diploid phase (see Section 13.5). Exceptions include certain simple organisms, such as Yeast (where only haploid cells undergo mitotic division, while a diploid cell, once formed, immediately enters meiosis), as well as plants, albeit to a lesser extent; in plants, mitotic divisions occur in both the Haploid and Diploid phases. However, in all plants except the most primitive ones, the haploid phase is extremely short and simple, whereas the diploid phase represents a prolonged period of GROWTH AND DEVELOPMENT. In nearly all multicellular animals, including all vertebrates, the haploid phase is even shorter. They spend virtually their entire life cycle in the diploid state; haploid cells are short-lived, do not divide at all, and are specially adapted for sexual fusion (Fig. 15-3).

The haploid cells that fuse during Fertilization are called Gametes. Typically, Two Types of gametes are formed: large, non-motile egg cells (or ova) and small, motile sperm cells (or spermatozoa) (Fig. 15-4). During the diploid phase, which begins immediately after gamete fusion, cells proliferate and specialize to form a complex multicellular organism. In most animals (though not plants), it is useful to distinguish between germ-line cells (the germ line), which give rise to the next generation of gametes, and somatic cells, which form the rest of the body and leave no progeny. In a sense, somatic cells exist solely to support the survival and reproduction of the germ-line cells (sex cells).

Fig. 15-2. The life cycle of a sexually reproducing organism involves the alternation of a diploid cell generation with a haploid one.

Fig. 15-3. This diagram illustrates how cells of higher eukaryotes proliferate in the diploid phase to form a multicellular organism, in which only the gametes are haploid. Conversely, in some lower eukaryotes, it is the haploid cells that proliferate, and the only diploid cell is the zygote, which exists for a very short time following fertilization. Haploid cells are highlighted in color.

Fig. 15-4. An egg cell of a bivalve mollusk with numerous sperm cells attached to its surface. Scanning electron micrograph. (Courtesy of David Epel.)

15.1.2. Sexual reproduction makes organisms competitive in a changing environment

The machinery of sexual reproduction is complex, and the metabolic costs involved are very high. What advantages does it confer, and why did it evolve? Through genetic recombination, parental organisms produce offspring that differ from them in highly unpredictable ways. Among these novel, random gene combinations, at least half may turn out to be inferior to the parental genotypes. If so, why should sexual reproduction be more advantageous than asexual reproduction, in which offspring retain all parental genes? Although population geneticists still do not fully understand this question, the core Conclusion appears to be that gene shuffling during sexual reproduction helps species survive in changing environments. If a parent produces many offspring with diverse gene combinations, There is a greater chance that at least one descendant will be well-suited to future life circumstances, whatever they may be. Many hypotheses have been proposed to explain the evolutionary advantages of sex in the Struggle for Existence. One of them offers insight into what the Cytology/cytology/16.html">Early stages of the evolution of sexual reproduction might have been like. Evolutionary progress largely depends on Mutations that alter existing genes to form new alleles (variants) of those genes. Suppose that two individuals in a population acquire beneficial mutations affecting different genetic loci and, consequently, different Functions.

In an asexual species, each of these individuals would give rise to a clone of mutant descendants, and the two new clones would compete until one outgrew the other. One of the beneficial mutant alleles would thus spread, while the other would eventually vanish. Now imagine that one of the original mutants possesses a genetically determined trait that enables it to occasionally incorporate genes from other cells into its genome. In the struggle for existence, acquiring genes from cells of a competing clone is equivalent to creating a cell that carries all the beneficial mutations. Such a cell would have superior fitness, and the resulting advantage would drive the spread of the gene-incorporation trait through the population. Natural Selection would favor this primitive form of sexual reproduction.

Whatever the origins of sexual reproduction, it is striking that the evolution of virtually all complex organisms alive today has proceeded through the alternation of numerous sexually reproducing generations. Despite the Abundance of asexual organisms, they appear to have remained quite primitive. Why? The answer may lie in the fact that sexual reproduction provides unique opportunities for genetic renewal, driving The Development of complex organisms. We will explore this further below.

15.1.3. New genes arise through duplication and divergence

The evolution of a complex organism requires more than just refining existing genes: it demands new genes to carry out novel functions. How do they arise?

Many Proteins in multicellular animals can be grouped into families: collagens, Globins, Serine proteases, and so on. Proteins within the same family are closely related both in function and in Amino Acid Sequence. There is little doubt that the protein genes of each such family descended from a single ancestral gene through processes of duplication and divergence (Section 10.5.3). Different members of a protein family are frequently characteristic of various body Tissues, where they perform similar yet slightly distinct functions. The generation of new genes via the divergence and specialization of existing ones clearly played a decisive role in the evolution of complex Multicellular Organisms. In this respect, diploid organisms possess a major advantage: they carry an extra copy of every gene, and this spare copy can mutate and serve as raw material for evolutionary innovation. Haploid species cannot as easily embark on the path leading to genome expansion and complexity. To understand The Mechanism of these processes, we need to examine The Link Between sexual reproduction and diploidy in somewhat greater detail.

15.1.4. Sexual reproduction maintains diploidy in diploid species

A diploid organism possesses two copies of every gene—one from each parent; however, in most cases, a single copy is sufficient for survival and normal physiological function. A mutation that disrupts the function of a vital gene is lethal to a haploid organism, but it may prove harmless

to a diploid if only one of the two gene copies is affected, i.e., if the organism is heterozygous for the mutation. As a rule, the genomes of diploid organisms harbor many recessive deleterious alleles. Often, heterozygous individuals exhibit slightly reduced fitness, which hinders the spread of such alleles. However, even when the fitness of heterozygotes is not impaired, sexual reproduction restricts the frequency of recessive lethals in a population (Fig. 15-5). If both parents carry a recessive lethal mutation in the same gene, their offspring may inherit two mutant copies of that gene and receive no normal ones; such a homozygous organism will perish, and the mutant gene copies will be lost with it. The more widespread a lethal allele is in a population, the faster it is eliminated. As a result, an equilibrium is established between The rate of lethal allele elimination and the rate at which it is generated by fresh mutations. At equilibrium, a recessive lethal allele occurs quite rarely in the population (though significantly more often than it would in a haploid organism): the overwhelming majority of individuals will possess two functional gene copies. A similar situation applies to recessive mutations that are simply deleterious (reducing offspring number) rather than lethal. In general, given sexual reproduction and genetic recombination, selection ensures that in most individuals, a majority of gene loci retain two functionally interchangeable copies, thereby preserving the diploid state of The Genome.

For comparison, consider a population initially consisting of diploid individuals that reproduce asexually. In the absence of genetic recombination, nothing prevents the two copies of each gene from evolving along separate pathways. Deleterious recessive mutations will accumulate in the genome until diploidy is replaced by a state where the total amount of DNA remains unchanged, but only a single functioning copy of each originally essential gene is retained. The organism becomes "functionally haploid." An idea of the time scales required for such evolutionary changes can be gleaned from studying the evolution of suckers (catostomid fish)¹. These fish descend from ancestors whose entire diploid genome underwent complete duplication roughly 50 million years ago, making them tetraploids. It is estimated that about 50% of the "extra" protein-coding gene pairs have lost their functional significance since that time.

¹⁾ Catostomids (Catostomidae) are a family of freshwater fish of the order Cypriniformes. — Ed.

15.1.5. A diploid species possesses an extra copy of every gene, which can mutate and subsequently acquire a new function

Most mutations are harmful because they disrupt gene functions that have already been optimized through natural selection. Occasionally, however, a mutation may modify an existing gene in such a way that it acquires a novel, useful function. Typically, such a mutation renders the gene incapable of carrying out its original function, and if this function was vital, the haploid organism dies. In a diploid organism, however, such a mutation in one of the two gene copies is not merely tolerated—it is advantageous. Even the slight benefits conferred upon the organism by the new mutant gene will be sufficient to outweigh the detriment caused by the loss of one of the two original gene copies: the heterozygous individual will reap the benefits of both the old and the new gene functions. Homozygotes carrying two copies of the old allele or two copies of the new one will be less fit. In such cases, where heterozygotes hold an advantage, the mutant gene spreads rapidly through a sexually reproducing diploid population until an equilibrium is reached in which both old and new alleles are present at high frequencies and the proportion of heterozygous individuals is large. This phenomenon is known as balanced polymorphism. There is a price to pay, however: when two heterozygotes mate, a significant fraction of their offspring, in accordance with standard Mendelian laws, will be homozygous and consequently less fit. Yet this state of affairs does not persist indefinitely—there is a way out.

Fig. 15-5. This diagram illustrates how diploid organisms maintain diploidy throughout evolution during sexual reproduction. For simplicity, only lethal recessive mutations are shown. Harmful recessive mutations follow a similar pattern.

15.1.6. A diploid species can rapidly enrich its genome by acquiring new genes

From time to time, all organisms undergo spontaneous Gene Duplication: a chromosome containing a single copy of gene G gives rise, as a result of a METABOLISM/36.html">DNA Replication error, to a chromosome containing two copies of this gene arranged in tandem. Such duplications confer no selective advantage on their own and are typically found in very few individuals. Suppose, however, that a duplication occurs at a locus containing a beneficial mutant allele G*, which is present at a high frequency in the population due to selection favoring heterozygotes and coexists in the genome with the original allele G (Fig. 15-6). It is then highly likely that in a diploid cell containing the GG chromosome (bearing the duplication), its homolog will carry the G* allele, resulting in the GG/G* genotype. Subsequently, as a result of genetic recombination during meiosis (see below), gametes with the GG* genotype can be formed. In these gametes, the original gene G and the mutant G*, located adjacent to each other, are no longer two alleles competing for the same locus; they are now two distinct genes, each occupying its own locus. Such a combination is advantageous and will spread rapidly until the entire population consists of GG*/GG* homozygotes (see Fig. 15-6). The advantage of individuals with this genotype lies not only in possessing both genes—the old G and the new G*—but also in their ability to pass this advantage on to all their descendants.

Thus, in a sexually reproducing diploid species, new genes can arise via mutations in extra copies of existing genes; these new genes can spread through the population driven by selection favoring heterozygotes, while the original genes are not lost; and finally, new genes can be stably incorporated into the genome through gene duplication and genetic recombination. This sequence of events is possible only in diploid species. Genome enrichment in haploid species is fraught with major difficulties. If a species is to acquire a new gene while retaining the old one, it must wait for the required mutation to occur in one of the very few individuals that have already undergone duplication of the corresponding locus. And since both mutations and duplications at a given locus are extremely rare events, a haploid species must wait an exceedingly long time for these events to coincide (Fig. 15-7). Detailed calculations show that—except in situations where the rate of gene duplication is very high—a diploid organism is capable of expanding its genome and adding new genes with novel functions hundreds or even thousands of times faster than a haploid organism. This difference is most pronounced for mutations that occur at a low frequency, precisely the kind of rare mutations required for genome renewal.

Fig. 15-6. Emergence of a new gene (G*) via the "mutation → spread → duplication" pathway during Sexual reproduction in a diploid organism.

Fig. 15-7. Generation of a new gene in a haploid organism. This sequence of events appears much simpler than the one shown in Fig. 15-6, but it requires significantly more time to be realized.

Thus, sexual reproduction goes hand in hand with diploidy, which in turn provides particularly favorable conditions for creating a larger, more complex, and more flexible genome. Of course, evolution can take many paths, and the route of gene duplication and divergence we have outlined is certainly not the only one. Nevertheless, sexual reproduction appears to have had a profound impact on the origins and modes of spread of genetic changes within populations, making possible the evolution of organisms as complex as ourselves.

We can now turn to a detailed Description of the cellular mechanisms of the sexual process. In the subsequent sections, we will first examine meiosis—the process during which genetic recombination takes place and haploid gametes are formed from diploid cells—then we will look at the gametes themselves, and finally we will explore fertilization, the process in which gametes fuse to form a new diploid organism.

Summary

Sexual reproduction involves a cyclic alternation of diploid and haploid states: a diploid cell divides by meiosis to yield haploid cells, and haploid cells fuse in pairs during fertilization to form new diploid cells. During this process, genomes are shuffled and recombined, producing individuals with novel gene combinations. Higher Plants and animals spend the major part of their life cycle in the diploid phase, whereas their haploid phase is very brief. Evolutionary pressures likely favored sexual reproduction because random genetic recombination increased the chances that at least some offspring would survive in an unpredictably changing world. The sexual process is also essential for maintaining diploidy, as it helps create the conditions necessary for the Structure/89.html">Rapid Evolution of new genes in higher plants and animals.