Origin and function of meiosis

Eukaryotes are organisms with a true nucleus in which the DNA genome is enclosed in a double membrane (e.g. fungi, protozoans, vertebrates, higher plants), in contrast to prokaryotes (bacteria and blue-green algae) that lack a nuclear membrane. It may seem surprising, given the enormous accomplishments of molecular and evolutionary biology, but there is still no general agreement among biologists on the questions of how sex in eukaryotes arose in evolution and what basic function sex serves. Fundamental to answering these questions is achieving an understanding of the origin and function of meiosis. Meiosis is a key stage of the sexual cycle in eukaryotes. Meiosis is the stage of the sexual cycle in which a diploid cell, ordinarily having two complete sets of chromosomes, gives rise to haploid cells (gametes) each having one set of chromosomes. Two such gametes arising from different individual organisms may fuse by the process of syngamy (fertilization) to generate a new diploid individual, thus completing the sexual cycle.

Meiosis is ubiquitous among eukaryotes. It occurs in single-celled organisms such as yeast, as well as in multicellular organisms, such as humans. Eukaryotes arose from prokaryotes more than 1.5 billion years ago,^[1] and the earliest eukaryotes were likely single-celled organisms. To understand sex in eukaryotes, it is necessary to understand (1) how meiosis arose in single celled eukaryotes, and (2) the function of meiosis.

Origin of Meiosis

There are two conflicting theories on how meiosis arose. One is that meiosis evolved from bacterial sex (called transformation) as bacteria evolved into eukaryotes. The other is that meiosis arose from mitosis.

Theory that meiosis evolved from bacterial sex (transformation)

In prokaryotic sex, DNA from one bacterium is released into the surrounding medium, is then taken up by another bacterium and its information integrated into the DNA of the recipient bacterium. This process is called transformation. One theory on how meiosis arose is that it evolved from transformation.^[2] By this view, the evolutionary transition from prokaryotic sex to eukaryotic sex was continuous.

Transformation, like meiosis, is a complex process requiring the function of numerous gene products. The ability to undergo natural transformation among bacterial species is widespread. At least 67 prokaryote species (in seven different phyla) are known to be competent for transformation.^[3] A key similarity between bacterial sex and eukaryotic sex is that DNA originating from two different individuals (parents) join up so that homologous sequences are aligned with each other, and this is followed by exchange of genetic information (a process called genetic recombination). After the new recombinant chromosome is formed it is passed on to progeny.

When genetic recombination occurs between DNA molecules originating from different parents, the recombination process is catalyzed in prokaryotes and eukaryotes by enzymes that have similar functions and that are evolutionarily related. One of the most important enzymes catalyzing this process in bacteria is referred to as RecA, and this enzyme has two functionally similar counterparts that act in eukaryotic meiosis, Rad51 and Dmc1.

Support for the theory that meiosis arose from bacterial transformation comes from the increasing evidence that early diverging lineages of eukaryotes have the core genes for meiosis. This implies that the precursor to meiosis was already present in the bacterial ancestor of eukaryotes. For instance the common intestinal parasite Giardia intestinalis, a simple eukaryotic protozoan was, until recently, thought to be descended from an early diverging eukaryotic lineage that lacked sex. However, it has since been shown that G. intestinalis contains within its genome a core set of genes that function in meiosis, including five genes that function only in meiosis.^[4] In addition, G. intestinalis was recently found to undergo a specialized, sex-like process involving meiosis gene homologs.^[5] This evidence, and other similar examples, suggest that a primitive form of meiosis, was present in the common ancestor of all eukaryotes, an ancestor that arose from antecedent bacteria.^[2][6]

Theory that meiosis evolved from mitosis

Mitosis is the process in eukaryotes for duplicating chromosomes and segregating each of the two copies into each of the two daughter cells upon somatic cell division (that is, during all cell divisions in eukaryotes, except those involving meiosis that give rise to haploid gametes). In mitosis, chromosome number is ordinarily not reduced. The alternate theory on the origin of meiosis is that meiosis evolved from mitosis.^[7] On this theory, early eukaryotes evolved mitosis first, but lacked meiosis and thus had not yet evolved the eukaryotic sexual cycle. Only after mitosis became established did meiosis and the eukaryotic sexual cycle evolve. The fundamental features of meiosis, on this theory, were derived from mitosis.

Support for the idea that meiosis arose from mitosis is the observation that some features of meiosis, such as the meiotic spindles that draw chromosome sets into separate daughter cells upon cell division, and processes regulating cell division employ the same, or similar, molecular machinery as employed in mitosis.

However, there is no compelling evidence for a period in the early evolution of eukaryotes during which meiosis and accompanying sexual capability was suspended. Presumably such a suspension would have occurred while the evolution of mitosis proceeded from the more primitive chromosome replication/segregation processes in ancestral bacteria until mitosis was established.

In addition, as noted by Wilkins and Holliday,^[7] there are four novel steps needed in meiosis that are not present in mitosis. These are: (1) pairing of homologous chromosomes, (2) extensive recombination between homologs; (3) suppression of sister chromatid separation in the first meiotic division; and (4) avoiding chromosome replication during the second meiotic division. They note that the simultaneous appearance of these steps appears to be impossible, and the selective advantage for separate mutations to cause these steps is problematic, because the entire sequence is required for reliable production of a set of haploid chromosomes.

Sharing of components during the evolution of meiosis and mitosis

On the view that meiosis arose from bacterial transformation, during the early evolution of eukaryotes, mitosis and meiosis could have evolved in parallel, with both processes using common molecular components. On this view, mitosis evolved from the molecular machinery used by bacteria for DNA replication and segregation, and meiosis evolved from the bacterial sexual process of transformation, but meiosis also made use of the evolving molecular machinery for DNA replication and segregation.

Function of Meiosis

Single-celled eukaryotes (protists) generally can reproduce asexually (vegetative reproduction) or sexually, depending on conditions. Asexual reproduction involves mitosis, and sexual reproduction involves meiosis. When sex is not an obligate part of reproduction, it is referred to as facultative sex. Present-day protists, generally, are facultative sexual organisms, as are many bacteria. The earliest form of sexual reproduction in eukaryotes was probably facultative, like that of present-day protists. To understand the function of meiosis in facultative sexual protists, we next consider under what circumstances these organisms switch from asexual to sexual reproduction, and what function this transition may serve.

Stress induces the eukaryotic sexual cycle in protists

Abundant evidence indicates that facultative sexual protists tend to undergo sexual reproduction under stressful conditions. For instance, the budding yeast Saccharomyces cerevisiae reproduces mitotically (asexually) as diploid cells when nutrients are abundant, but switches to meiosis (sexual reproduction) under starvation conditions.^[8] The unicellular green alga, Chlamydomonas reinhardi grows as vegetative cells in nutrient rich growth medium, but depletion of a source of nitrogen in the medium leads to gamete fusion, zygote formation and meiosis.^[9] The fissioning yeast Schizosaccharomyces pombe, treated with H2O2 to cause oxidative stress, substantially increases the proportion of cells which undergo meiosis.^[10] The simple multicellular eukaryote Volvox carteri undergoes sex in response to oxidative stress^[11] or stress from heat shock.^[12] These examples, and others, indicate that, in protists and simple multicellular eukaryotes, meiosis is an adaptation to deal with stress.

Stress induces sex in bacteria

Bacterial sex (transformation) also appears to be an adaptation to stress. For instance, transformation occurs near the end of logarithmic growth, when amino acids become limiting in Bacillus subtilis,^[13] or in Haemophilus influenzae when cells are grown to the end of logarithmic phase.^[14] In Streptococcus mutans and other streptococci, transformation is associated with high cell density and biofilm formation.^[15] In Streptococcus pneumoniae, transformation is induced by the DNA damaging agent mitomycin C.^[16] These, and other, examples indicate that bacterial transformation, like eukaryote meiosis in protists, is an adaptation to stressful conditions. This observation suggests that the natural selection pressures maintaining meiosis in protists are similar to the selective pressures maintaining bacterial transformation. This similarity further indicates continuity, rather than a gap, in the evolution of sex from bacteria to eukaryotes.

Theory that DNA repair is the adaptive advantage of meiosis

Stress is, however, a general concept. What is it specifically about stress that needs to be overcome by meiosis? And what is the specific benefit provided by meiosis that enhances survival under stressful conditions?

Again there are two contrasting theories. On one theory, meiosis is primarily an adaptation for repairing DNA damage. Environmental stresses often lead to oxidative stress within the cell, which is well known to cause DNA damage through the production of reactive forms of oxygen, known as reactive oxygen species (ROS). DNA damages, if not repaired, can kill a cell by blocking DNA replication, or transcription of essential genes.

When only one strand of the DNA is damaged, the lost information (nucleotide sequence) can ordinarily be recovered by repair processes that remove the damaged sequence and fill the resulting gap by copying from the opposite intact strand of the double helix. However, ROS also cause a type of damage that is difficult to repair, referred to as double-strand damage. One common example of double-strand damage is the double-strand break. In this case, genetic information (nucleotide sequence) is lost from both strands in the damaged region, and proper information can only be obtained from another intact chromosome homologous to the damage chromosome. The process that the cell uses to accurately accomplish this type of repair is called recombinational repair.

Meiosis is distinct from mitosis in that a central feature of meiosis is the alignment of homologous chromosomes followed by recombination between them. The two chromosomes which pair are referred to as non-sister chromosomes, since they did not arise simply from the replication of a parental chromosome. Recombination between non-sister chromosomes at meiosis is known to be a recombinational repair process that can repair double-strand breaks and other types of double-strand damage. In contrast, recombination between sister chromosomes cannot repair double-strand damages arising prior to the replication which produced them. Thus on this view, the adaptive advantage of meiosis is that it facilitates recombinational repair of DNA damages that are otherwise difficult to repair, and that occur as a result of stress, particularly oxidative stress.^[17][18] If left unrepaired, these damages would likely be lethal to gametes and inhibit production of viable progeny.

Even in multicellular eukaryotes, such as humans, oxidative stress is a problem for cell survival. In this case, oxidative stress is a byproduct of oxidative cellular respiration occurring during metabolism in all cells. In humans, on average, about 50 DNA double-strand breaks occur per cell in each cell generation.^[19] Meiosis, which facilitates recombinational repair between non-sister chromosomes, can efficiently repair these prevalent damages in the DNA passed on to germ cells, and consequently prevent loss of fertility in humans. Thus on the theory that meiosis arose from bacterial transformation, recombinational repair is the selective advantage of meiosis in both single celled eukaryotes and muticellular eukaryotes, such as humans.

Theory that genetic diversity is the adaptive advantage of sex

On the other view, stress is a signal to the cell that it is experiencing a change in the environment to a more adverse condition. Under this new condition, it may be beneficial to produce progeny that differ from the parent in their genetic make up. Among these varied progeny, some may be more adapted to the changed condition than their parents. Meiosis generates genetic variation in the diploid cell, in part by the exchange of genetic information between the pairs of chromosomes after they align (recombination). Thus, on this view,^[20] the advantage of meiosis is that it facilitates the generation of genomic diversity among progeny, allowing adaptation to adverse changes in the environment.

However, as also pointed out by Otto and Gerstein,^[20] in the presence of a fairly stable environment, individuals surviving to reproductive age have genomes that function well in their current environment. They raise the question of why such individuals should risk shuffling their genes with those of another individual, as occurs during meiotic recombination? Considerations such as this have led many investigators to question whether genetic diversity is the adaptive advantage of sex.

Summary

The two contrasting views on the origin of meiosis are (1) that it evolved from the bacterial sexual process of transformation and (2) that it evolved from mitosis. The two contrasting views on the fundamental adaptive function of meiosis are: (1) that it is primarily an adaptation for repairing damage in the DNA to be transmitted to progeny and (2) that it is primarily an adaptation for generating genetic variation among progeny. At present, these differing views on the origin and benefit of meiosis are not resolved among biologists.

See also

• DNA repair
• Evolution of sexual reproduction
• Fertilization
• Genetic recombination
• Giardia
• Meiosis
• Mitosis
• Oxidative stress

References

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