Frozen Evolution. Or, that’s not the way it is, Mr. Darwin. A Farewell to Selfish Gene.

Meiosis is a process that should theoretically ensure that homologous chromosomes from the original diploid chromosome set of maternal cells enter the haploid chromosome set of sex cells entirely at random regardless of the alleles that the individual chromosomes contain. However, in actual fact, this is frequently not true and the structure and gene content of the individual chromosomes frequently affect which of the pair of homologous chromosomes finally ends up in the sex cells and which does not. The process of differential transfer of genes to the sex cells through differential transfer of the individual chromosomes is called meoitic drive (Zimmering, Sandler, & Nicoletti 1970; Prout, Bundgaard, & Bryant 1973; Thomson & Feldman 1974).In most cases, meoitic drive occurs during meiosis; however, in some cases, the relevant processes already occur during mitosis, which precedes meiosis or, to the contrary, follows it. To the present day, a number of processes that lead to the origin of meiotic drive have been described.

Meiotic drive occurs very frequently in egg formation. During this process, only one haploid set of chromosomes ends up in the nucleus of the female gamete, while the remaining three sets are eliminated into the polar bodies. In heterozygote females, it very frequently occurs that the probability with which a certain allele will end up in the nucleus of the oocyte or in the polar body, i.e. the probability with which the allele will be transferred to the next generation, differ considerably (Fig. VI.10). (Crow 1979). In some cases a certain allele of a specific gene is proliferated in this way in the population while, in a different case, this can be a certain chromosome mutation (Ruvinsky 1995). If, for example, a laboratory mouse is crossed with a wild house mouse, whose karyotype contains a metacentric chromosome formed through Robertson translocation, i.e. fusion of two acrocentric chromosomes, it has been observed in five cases out of ten that the metacentric chromosome occurs in less than 50% of the progeny of heterozygote females. In some cases, the ratio of the two types of oocyte was as much as 3:1. The authors assumed that the metacentric chromosome would most probably end up in the primary polar body. In another study, monitoring the behaviour of a metacentric chromosome in a population of wild mice, it was observed, on the other hand, that the metacentric chromosome had the greatest probability of ending up in the nucleus of the oocyte (King 1993).

Similar phenomena were also observed for other organisms. For example, it has been observed in sorrel (Rumex acetosa) that only four of nine randomly selected chromosome mutations of the reciprocal translocation type or mutations externally manifested as a shift in centromers exhibited normal Mendelian heredity. In the remaining five, meoitic drive appeared to some degree, in the female or the male plants.

DNA sequencing in the area of the centromere (the site of attachment of microtubules of meiotic spindle and therefore probably an important battlefield for meiotic distorters) in closely related species indicated that these areas are subject to very rapid evolution. It is highly probable that this is the result of a battle between genetic elements proliferating through meoitic drive. According to some authors, a significant part of the DNA in the area around the centromere is formed of these active or inactive elements – meiotic distorters. The predominance of nonsynonymous mutations in the histones that are bonded to the DNA in the area of the centromere, is interpreted in a similar way (a battle between meiotic distorters).Meiotic drive occurs very frequently in egg formation. During this process, only one haploid set of chromosomes ends up in the nucleus of the female gamete, while the remaining three sets are eliminated into the polar bodies. In heterozygote females, it very frequently occurs that the probability with which a certain allele will end up in the nucleus of the oocyte or in the polar body, i.e. the probability with which the allele will be transferred to the next generation, differ considerably (Fig. VI.10). (Crow 1979). In some cases a certain allele of a specific gene is proliferated in this way in the population while, in a different case, this can be a certain chromosome mutation (Ruvinsky 1995). If, for example, a laboratory mouse is crossed with a wild house mouse, whose karyotype contains a metacentric chromosome formed through Robertson translocation, i.e. fusion of two acrocentric chromosomes, it has been observed in five cases out of ten that the metacentric chromosome occurs in less than 50% of the progeny of heterozygote females. In some cases, the ratio of the two types of oocyte was as much as 3:1. The authors assumed that the metacentric chromosome would most probably end up in the primary polar body. In another study, monitoring the behaviour of a metacentric chromosome in a population of wild mice, it was observed, on the other hand, that the metacentric chromosome had the greatest probability of ending up in the nucleus of the oocyte (King 1993).

Similar phenomena were also observed for other organisms. For example, it has been observed in sorrel (Rumex acetosa) that only four of nine randomly selected chromosome mutations of the reciprocal translocation type or mutations externally manifested as a shift in centromers exhibited normal Mendelian heredity. In the remaining five, meoitic drive appeared to some degree, in the female or the male plants.

DNA sequencing in the area of the centromere (the site of attachment of microtubules of meiotic spindle and therefore probably an important battlefield for meiotic distorters) in closely related species indicated that these areas are subject to very rapid evolution. It is highly probable that this is the result of a battle between genetic elements proliferating through meoitic drive. According to some authors, a significant part of the DNA in the area around the centromere is formed of these active or inactive elements – meiotic distorters. The predominance of nonsynonymous mutations in the histones that are bonded to the DNA in the area of the centromere, is interpreted in a similar way (a battle between meiotic distorters).

Another way in which an allele can spread through meoitic drive consists in programming the chromosome that carries the alternative allele to destroy or damage the gamete in which it will end up after the completion of meoisis. This mechanism occurs, e.g. in known systems in the fruit fly Drosophila melanogaster (segregation distortion, SD-systém) and in the house mouse Mus musculus (t-haplotype) (Carvalho & Vaz 1999; Ardlie 1998; Vanboven et al. 1996) (Fig. IV.11). In both cases, meiotic drive occurs during sperm formation and, in both cases, this leads to a smaller number of viable sperm in the ejaculate of a heterozygote male and, in both cases, most of the viable sperm contain the allele that causes this effect. Simultaneously, the destruction of the sex cells containing the normal allele is an active process from the standpoint of the normal allele. If the relevant chromosome does not contain the normal allele in the relevant locus because of deletion, the sperm is not destroyed. This means that the allele responsible for meiotic drive somehow manages to reprogram the normal allele so that, after completion of cell division, it actively damages the spermatid or sperm, in which the nucleus is located. However, it is a certain simplification to speak of an allele in this case; in actual fact, the relevant “allele” consists of a combination of several genes in closely adjacent loci.

The mechanism of meiosis should ensure, amongst other things, that the members of a heterogamete sex will produce the same number of gametes with two different sets of sex chromosomes and thus the ratio of males and females in their progeny will equal 1:1. However, for a number of species, populations are known in which the ratio of males and females differs substantially from the theoretical ratio of 1:1. In some cases, meiotic drive is responsible for this deviation (Carvalho & Vaz 1999). Alleles proliferating in the gene pool through the action of this mechanism are denoted as SRD (sex ratio distorters). For example, in the mosquito Aedes aegypti, gene D (distorter), whose active allele causes decomposition of the X-chromosomes in future sperm, is located on the Y-chromosome close to gene M, i.e. the gene that determines male sex. Males with active allele D thus produce far fewer viable sperm, and most of them contain a Y-chromosome and thus lead to the formation of males. The SRD system on the X-chromosome of several species of drosophila acts similarly, but in the opposite direction.

The distortion of the sex ratio in favour of males (Aedes) or in favour of females (Drosophila) can, of course, seriously affect the existence of the population. According to some authors, in many species this process can substantially affect the behaviour of the entire meta-population, specifically the rate of formation and disappearance of local subpopulations (Carvalho & Vaz 1999).

Large evolutionary plasticity and the great variety of genetic sex-determining mechanisms is currently explained by the existence of the selection pressure of the SRD-allele, specifically the necessity from time to time of formation of substitute mechanisms capable of compensating the distorted sex ratio that occurs with proliferation of certain SRD alleles (Werren & Beukeboom 1998).

It has been estimated that more than 90% of speciation events are accompanied by the formation of a modified karyotype in a daughter species (White 1978). It is probable that, in the case of allopatric speciation, meiotic drive is responsible for this phenomenon or, to be more exact, the fact that the karyotype of the species changes much faster through the effect of meiotic drive than new species are formed. Speciation events only conserve differences in the gene pool of the two populations existing at the given instant and simultaneously create a barrier capable of preventing spreading of chromosome mutations from one population to another. Thus, the karyotypes of two daughter species can diverge. As this divergence occurs through the effect of relatively fast meiotic drive, divergence of karyotypes occurs faster than divergence of phenotypes, which change through the action of the slower processes of genetic drift and selection.

However, in the case of sympatric speciation, it is assumed that meiotic drive could sometimes participate directly in the creation of species barriers and that it could thus actively contribute to the origin of new species. If Robertsonian translocations gradually spread from various areas in the  area occupied by a given species, this entire area can disintegrate into a number of separate areas, where individuals of a different chromosomal race will live in each of them. The boundaries between these areas can be very sharp, especially if two races are next to one another, whose karyotypes contain two different Robertsonian translocations, in which the same acrocentric chromosome, as one of the pair of fused chromosomes, is present (see Fig. XXI.12). Because of the common branch, the two different metacentric chromosomes participate in creation of a chromosome tetrade during meiosis in  hybrids between the two races. Subsequently, disorders occur in the transfer of the chromosomes to the fields of the meiotic spindle and a substantial percentage of nonfunctional gametes is formed. In species in which more intense sperm competition occurs, because the female is often rapidly fertilized by several males in succession, the amount and quality of the sperm in the ejaculate or spermatheca decide the paternity of the individual embryos to a substantial degree. In this case, the heterozygote sons of a male that penetrated into the area of occurrence of a different chromosomal race have substantially reduced biological fitness. This can form a relatively effective barrier against spreading of metacentric chromosomes from the area of one chromosome race into the area of another. Because of the existence of crossing-over, such a barrier need not prevent the flux of the individual genes (or, to be more exact, alleles) between sympatric or parapatric (adjacent) populations of the two chromosome races.  However, reduced fertility of heterozygotes can create very strong selection pressure for the formation of specific recognition mechanisms, capable of preventing mutual crossing of the members of two different chromosome races. If the genes affecting this recognition occur in the area of chromosomes in which crossing-over does not occur for some reason, for example, in the inversion area, it is highly probable that meiotic drive will lead to the formation of two separate species.

Some authors (Ridley 2000)are of the opinion that meiotic drive is an extremely important evolution factor, where the effect of this factor on the average biological fitness of the members of the population is almost always negative. Meiotic drive could be manifested especially strongly in organisms in which crossing-over would not exist and in which alleles would thus not be mixed in pairs of homologous chromosomes. Competition of the individual chromosomes for the most effective spreading in the gene pool of the population through meiotic drive in these cases could generally predominate over competition between the individual alleles for the most effective transfer to further generations through the positive effect on the biological fitness of their bearers, i.e. over natural selection. Crossing-over, which breaks up alliances of alleles of individual chromosomes, is a very effective mechanism limiting the action of meiotic drive, and its development in evolution may even be a necessary condition for the existence of sexual reproduction based on meiosis and syngamy (Haig & Grafen 1991).