Relative effects of segregation and recombination on the evolution of sex in finite diploid populations

The mechanism of reproducing more viable offspring in response to selection is a major factor influencing the advantages of sex. In diploids, sexual reproduction combines genotype by recombination and segregation. Theoretical studies of sexual reproduction have investigated the advantage of recombination in haploids. However, the potential advantage of segregation in diploids is less studied. This study aimed to quantify the relative contribution of recombination and segregation to the evolution of sex in finite diploids by using multilocus simulations. The mean fitness of a sexually or asexually reproduced population was calculated to describe the long-term effects of sex. The evolutionary fate of a sex or recombination modifier was also monitored to investigate the short-term effects of sex. Two different scenarios of mutations were considered: (1) only deleterious mutations were present and (2) a combination of deleterious and beneficial mutations. Results showed that the combined effects of segregation and recombination strongly contributed to the evolution of sex in diploids. If deleterious mutations were only present, segregation efficiently slowed down the speed of Muller''s ratchet. As the recombination level was increased, the accumulation of deleterious mutations was totally inhibited and recombination substantially contributed to the evolution of sex. The presence of beneficial mutations evidently increased the fixation rate of a recombination modifier. We also observed that the twofold cost of sex was easily to overcome in diploids if a sex modifier caused a moderate frequency of sex.     

Sex in Cheese: Evidence for Sexuality in the Fungus Penicillium roqueforti

Although most eukaryotes reproduce sexually at some moment of their life cycle, as much as a fifth of fungal species were thought to reproduce exclusively asexually. Nevertheless, recent studies have revealed the occurrence of sex in some of these supposedly asexual species. For industrially relevant fungi, for which inoculums are produced by clonal-subcultures since decades, the potentiality for sex is of great interest for strain improvement strategies. Here, we investigated the sexual capability of the fungus Penicillium roqueforti, used as starter for blue cheese production. We present indirect evidence suggesting that recombination could be occurring in this species. The screening of a large sample of strains isolated from diverse substrates throughout the world revealed the existence of individuals of both mating types, even in the very same cheese. The MAT genes, involved in fungal sexual compatibility, appeared to evolve under purifying selection, suggesting that they are still functional. The examination of the recently sequenced genome of the FM 164 cheese strain enabled the identification of the most important genes known to be involved in meiosis, which were found to be highly conserved. Linkage disequilibria were not significant among three of the six marker pairs and 11 out of the 16 possible allelic combinations were found in the dataset. Finally, the detection of signatures of repeat induced point mutations (RIP) in repeated sequences and transposable elements reinforces the conclusion that P. roqueforti underwent more or less recent sex events. In this species of high industrial importance, the induction of a sexual cycle would open the possibility of generating new genotypes that would be extremely useful to diversify cheese products.     

A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis

Sexual reproduction in eukaryotes is accomplished by meiosis, a complex and specialized process of cell division that results in haploid cells (e.g., gametes). The stereotypical reductive division in meiosis is a major evolutionary innovation in eukaryotic cells, and delineating its history is key to understanding the evolution of sex. Meiosis arose early in eukaryotic evolution, but when and how meiosis arose and whether all eukaryotes have meiosis remain open questions. The known phylogenetic distribution of meiosis comprises plants, animals, fungi, and numerous protists. Diplomonads including Giardia intestinalis (syn. G. lamblia) are not known to have a sexual cycle; these protists may be an early-diverging lineage and could represent a premeiotic stage in eukaryotic evolution. We surveyed the ongoing G. intestinalis genome project data and have identified, verified, and analyzed a core set of putative meiotic genes-including five meiosis-specific genes-that are widely present among sexual eukaryotes. The presence of these genes indicates that: (1) Giardia is capable of meiosis and, thus, sexual reproduction, (2) the evolution of meiosis occurred early in eukaryotic evolution, and (3) the conserved meiotic machinery comprises a large set of genes that encode a variety of component proteins, including those involved in meiotic recombination.     

Influences of Dominance and Evolution of Sex in Finite Diploid Populations

Most eukaryotes reproduce sexually. Although the benefits of sex in diploids mainly stem from recombination and segregation, the relative effects of recombination and segregation are relatively less known. In this study, we adopt an infinite loci model to illustrate how dominance coefficient of mutations affects the above-mentioned genetic events. However, we assume mutational effects to be independent and also ignore the effects of epistasis within loci. Our simulations show that with different levels of dominance, segregation and recombination may play different roles. In particular, recombination more commonly has a major impact on the evolution of sex when deleterious mutations are partially recessive. In contrast, when deleterious mutations are dominant, segregation becomes more important than recombination, a finding that is consistent with previous studies stating that segregation, rather than recombination, is more likely to drive the evolution of sex. Moreover, beneficial mutations alone remarkably increases the effects of recombination. We also note that populations favor sexual reproduction when deleterious mutations become more dominant or beneficial mutations become more recessive. Overall, these results illustrate that the existence of dominance is an important mechanism that affects the evolution of sex.     

The evolution of sex: empirical insights into the roles of epistasis and drift

Despite many years of theoretical and experimental work, the explanation for why sex is so common as a reproductive strategy continues to resist understanding. Recent empirical work has addressed key questions in this field, especially regarding rates of mutation accumulation in sexual and asexual organisms, and the roles of negative epistasis and drift as sources of adaptive constraint in asexually reproducing organisms. At the same time, new ideas about the evolution of sexual recombination are being tested, including intriguing suggestions of an important interplay between sex and genetic architecture, which indicate that sex and recombination could have affected their own evolution.     

Imperfect Genes, Fisherian Mutation and the Evolution of Sex

In this paper we present a mathematical model of mutation and selection that allows for the coexistence of multiple alleles at a locus with very small selective differences between alleles. The model also allows for the determination of fitness by multiple loci. Models of this sort are biologically plausible. However, some previous attempts to construct similar models have assumed that all mutations produce a decrease in fitness, and this has led to a tendency for the average fitness of population members to decline when population numbers are finite. In our model we incorporate some of the ideas of R. A. FISHER, so that both deleterious and beneficial mutations are possible. As a result, average fitness tends to approach a stationary distribution. We have used computer simulation methods to apply the Fisherian mutation model to the problem of the evolution of sex and recombination. The results suggest that sex and recombination can provide very large benefits in terms of average fitness. The results also suggest that obligately sexual species will win ecological competitions with species that produce a substantial fraction of their offspring asexually, so long as the number of sites under selection within the genomes of the competing species is not too small and the population sizes are not too large. Our model focuses on fertility selection in an hermaphroditic plant. However, the results are likely to generalize to a wide variety of other situations as well.     

Tetrahymena meiosis: Simple yet ingenious

The presence of meiosis, which is a conserved component of sexual reproduction, across organisms from all eukaryotic kingdoms, strongly argues that sex is a primordial feature of eukaryotes. However, extant meiotic structures and processes can vary considerably between organisms. The ciliated protist Tetrahymena thermophila, which diverged from animals, plants, and fungi early in evolution, provides one example of a rather unconventional meiosis. Tetrahymena has a simpler meiosis compared with most other organisms: It lacks both a synaptonemal complex (SC) and specialized meiotic machinery for chromosome cohesion and has a reduced capacity to regulate meiotic recombination. Despite this, it also features several unique mechanisms, including elongation of the nucleus to twice the cell length to promote homologous pairing and prevent recombination between sister chromatids. Comparison of the meiotic programs of Tetrahymena and higher multicellular organisms may reveal how extant meiosis evolved from proto-meiosis.     

Extensive Divergence Between Mating-Type Chromosomes of the Anther-Smut Fungus

Genomic regions that determine mating compatibility are subject to distinct evolutionary forces that can lead to a cessation of meiotic recombination and the accumulation of structural changes between members of the homologous chromosome pair. The relatively recent discovery of dimorphic mating-type chromosomes in fungi can aid the understanding of sex chromosome evolution that is common to dioecious plants and animals. For the anther-smut fungus, Microbotryum lychnidis-dioicae (= M. violaceum isolated from Silene latifolia), the extent of recombination cessation on the dimorphic mating-type chromosomes has been conflictingly reported. Comparison of restriction digest optical maps for the two mating-type chromosomes shows that divergence extends over 90% of the chromosome lengths, flanked at either end by two pseudoautosomal regions. Evidence to support the expansion of recombination cessation in stages from the mating-type locus toward the pseudoautosomal regions was not found, but evidence of such expansion could be obscured by ongoing processes that affect genome structure. This study encourages the comparison of forces that may drive large-scale recombination suppression in fungi and other eukaryotes characterized by dimorphic chromosome pairs associated with sexual life cycles.     

Molecular cloning and sexually dimorphic expression of DM-domain genes in Daphnia magna

Daphnia magna is known to switch between sexual and asexual reproduction depending on the environment. It reproduces asexually when in an optimal environment for food, photoperiod, and population density. Once the environment declines, it changes reproductive strategy from asexual to sexual reproduction. However, the molecular bases of environmental sex determination are largely unknown. To understand the molecular mechanisms of environmental sex determination in Daphnia, it is essential to isolate the genes related to sex determination. As DM-domain genes are well known as sex-related genes, we aimed to identify DM-domain genes from Daphnia. Based on degenerate PCR of conserved DM domains using Daphnia cDNA, we identified three DM-domain genes that corresponded to DMRT11E, DMRT93B, and DMRT99B of Drosophila melanogaster. Quantitative gene expression analysis in gonads revealed that DMRT93B was expressed only in the testis. This finding contributes to an improved understanding of the switching mechanism from an asexual to a sexual life cycle depending on the environment.     

Variation and Evolution of Meiosis

Meiosis arose in the evolution of primitive unicellular organisms as a part of sexual process. One type of meiosis, the so-called classical type, predominates in all kingdoms of eukaryotes. Meiosis is controlled by hundreds of genes, both shared with mitosis and specifically meiotic ones. In a wide range of taxa, which in some cases include kingdoms, meiotic genes and features obey Vavilov's law of homologous variation series. Synaptonemal complexes (SCs) temporarily binding homologous chromosomes at prophase I, ensure precise and equal crossing over and interference. SC proteins have 60–80% homology within the class of mammals but differ from the corresponding proteins in fungi and insects. Thus, nonhomologous SC proteins perform similar functions in different taxa. Some recombination enzymes in fungi and plants have common epitopes. The molecular mechanism of recombination is inherited by eukaryotes from prokaryotes and operates in special compartments: SC recombination nodules. Chiasmata, i.e., physical crossovers of nonsister chromatids, are preserved in bivalents until metaphase I due to local cohesion of sister chromatids in the remaining SC fragments. Owing to chiasmata, homologous chromosomes participate in meiosis I in pairs rather than individually, which, along with unipolarity of kinetochores (only in meiosis 1), ensures segregation of homologous chromosomes. The appearance of SC and chiasmata played a key role in the evolution of unicellular organisms since it promoted the development of a progressive type of meiosis. Some lower eukaryotes retain primitive meiosis types. These primitive modes of meiosis also occur in the sex of some insects that is heterozygous for sex chromosomes. I suggest an explanation for these cases. Mutations at meiotic genes impair meiosis; however, due to the preservation of archaic meiotic genes in the genotype, bypass metabolic pathways arise, which provide partial rescue of the traits damaged by mutations. Individual blocks of genetic program of meiotic regulation have probably evolved independently.     

The costs of sex due to deleterious intracellular parasites

A major problem in evolutionary theory is to explain the widespread occurrence of sexual recombination. This is particularly difficult in anisogamous species where the familiar ‘two-fold cost of sex’ is encountered. Another cost has recently been identified: that fusion of gametes allows intracellular parasites or deleterious ‘selfish’ genomes to invade a population. These costs of anisogamy and the ability of cytoplasmic agents to invade a sexual population are quantified, allowing the costs and consequences of different modes of reproduction to be compared. It is found that the costs of selfish elements are likely to be very high and, in particular, that isogamous sexual reproduction (the putative ‘primitive’ form) is not cost-free, but incurs a fitness reduction of the order of 90%; thus a large selective disadvantage occurs in the initial evolution of sex which is ignored in standard analysis. Even once anisogamy has evolved, the low levels of ‘paternal leakage’ observed in many extant organisms may allow selfish cytoplasmic elements to spread, resulting in moderate to large decreases in host population fitness. However, much of the cost of selfish elements is avoided in sexual lifecycles with a large number of asexual cellular divisions between sexual reproduction: this greatly impedes the spread of selfish agents and reduces the fitness loss attributable to selfish elements.     

Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae

Trade-offs between life-history components are a central concept of evolution and ecology. Sexual and natural selection seem particularly apt to impose antagonistic selective pressures. When sex is not integrated into reproduction, as in Saccharomyces cerevisiae, natural selection can impair or even eliminate it. In this study, a genetic trade-off between the sexual and asexual phases of the yeast life cycle was suggested by sharp declines in the mating and sporulation abilities of unrelated genotypes that were propagated asexually in minimal growth medium and in mice. When sexual selection was applied to populations that had previously evolved asexually, sexual fitness increased but asexual fitness declined. No such negative correlation was observed when sexual selection was applied to an ancestral strain: sexual and asexual fitness both increased. Thus, evolutionary history affected the evolution of genetic correlations, as fitness increases in a population already well adapted to the environment were more likely to come at the expense of sexual functions.     

Variation and evolution of meiosis

Meiosis arose in the evolution of primitive unicellular organisms as a part of sexual process. One type of meiosis, the so-called classical type, predominates in all kingdoms of eukaryotes. Meiosis is controlled by hundreds of genes, both shared with mitosis and specifically meiotic ones. In a wide range of taxa, which in some cases include kingdoms, meiotic genes and features obey Vavilov's law of homologous variation series. Synaptonemal complexes (SCs) temporarily binding homologous chromosomes at prophase I, ensure precise and equal crossing over and interference. SC proteins have 60-80% homology within the class of mammals but differ from the corresponding proteins in fungi and plants. Thus, nonhomologous SC proteins perform similar functions in different taxa. Some recombination enzymes in fungi and insects have common epitopes. The molecular mechanism of recombination is inherited by eukaryotes from prokaryotes and operates in special compartments: SC recombination nodules. Chiasmata, i.e., physical crossovers of nonsister chromatids, are preserved in bivalents until metaphase I due to local cohesion of sister chromatids in the remaining SC fragments. Owing to chiasmata, homologous chromosomes participate in meiosis I in pairs rather than individually, which, along with unipolarity of kinetochores (only in meiosis 1), ensures segregation of homologous chromosomes. The appearance of SC and chiasmata played a key role in the evolution of unicellular organisms since it promoted the development of a progressive type of meiosis. Some lower eukaryotes retain primitive meiosis types. These primitive modes of meiosis also occur in the sex of some insects that is heterozygous for sex chromosomes. I suggest an explanation for these cases. Mutations at meiotic genes impair meiosis; however, due to the preservation of archaic meiotic genes in the genotype, bypass metabolic pathways arise, which provide partial rescue of the traits damaged by mutations. Individual blocks of genetic program of meiotic regulation have probably evolved independently.     

The First Sexual Lineage and the Relevance of Facultative Sex

Models for the origin of the sex incorporate either obligate or facultative sexual cycles. The relevance of each assumption to the ancestral sexual population can be examined by surveying the sexual cycles of eukaryotes, and by determining the first lineage to diverge after sexuality evolved. Two protistan groups, the parabasalids and the oxymonads, have been suggested to be early-branching sexual lineages. A maximum-likelihood analysis of elongation factor-1α sequences shows that the parabasalids diverged prior to the oxymonads and thus represent the earliest sexual lineage of eukaryotes. Since both of these protist lineages and most other eukaryotes are facultatively sexual, it is likely that the common ancestor of all known eukaryotes was facultatively sexual as well. This finding has important implications for the ``Best-Man hypothesis' and other models for the origin of sex. Received: 21 August 1998 / Accepted: 26 December 1998     

Sex and speciation: The paradox that non-recombining DNA promotes recombination

The benefits of sexual reproduction that outweigh its costs have long puzzled biologists. Increased genetic diversity generated by new allelic combinations, as enhanced by recombination during meiosis, is considered a primary benefit of sex. Sex-determining systems have evolved independently on numerous occasions. One of the most familiar is the use of sex chromosomes in vertebrates. Other eukaryotic groups also use sex chromosomes or smaller sex-determining regions within their chromosomes, such as the mating type loci in the fungi. In these organisms, sexual reproduction and its associated meiotic recombination are controlled by regions of the genome that are themselves blocked in recombination. Non-recombining DNA that is essential for recombination presents a paradox. One hypothesis is that sex-determination requires or leads to highly diverse alleles, establishing this block in recombination. A second hypothesis to account for the common occurrence of these types of sex-determining systems is that they combine mechanisms for recombination suppression and reproductive isolation, thereby promoting the evolution of new species. The fungal kingdom represents the ideal eukaryotic lineage to elucidate the functions of non-recombining regions in sex-determination and speciation.     

Origin of sex

The competitive advantage of sex consists in being able to use redundancy to recover lost genetic information while minimizing the cost of redundancy. We show that the major selective forces acting early in evolution lead to RNA protocells in which each protocell contains one genome, since this maximizes the growth rate. However, damages to the RNA which block replication and failure of segregation make it advantageous to fuse periodically with another protocell to restore reproductive ability. This early, simple form of genetic recovery is similar to that occurring in extant segmented single stranded RNA viruses. As duplex DNA became the predominant form of the genetic material, the mechanism of genetic recovery evolved into the more complex process of recombinational repair, found today in a range of species. We thus conclude that sexual reproduction arose early in the evolution of life and has had a continuous evolutionary history. We cite reasons to reject arguments for gaps in the evolutionary sequence of sexual reproduction based on the presumed absence of sex in the cyanobacteria. Concerning the maintenance of the sexual cycle among current organisms, we take care to distinguish between the recombinational and outbreeding aspects of the sexual cycle. We argue that recombination, whether it be in outbreeding organisms, self-fertilizing organisms or automictic parthenogens, is maintained by the advantages of recombinational repair. We also discuss the role of DNA repair in maintaining the outbreeding aspects of the sexual cycle.