Role of recombination and faithfulness to partner in sex chromosome degeneration

Abstract

Sex determination in mammals is strongly linked to sex chromosomes. In most cases, females possess two copies of X chromosome while males have one X and one Y chromosome. It is assumed that these chromosomes originated from a pair of homologous autosomes, which diverged when recombination between them was suppressed. However, it is still debated why the sex chromosomes stopped recombining and how this process spread out over most part of the chromosomes. To study this problem, we developed a simulation model, in which the recombination rate between the sex chromosomes can freely evolve. We found that the suppression of recombination between the X and Y is spontaneous and proceeds very quickly during the evolution of population, which leads to the degeneration of the Y in males. Interestingly, the degeneration happens only when mating pairs are unfaithful. This evolutionary strategy purifies the X chromosome from defective alleles and leads to the larger number of females than males in the population. In consequence, the reproductive potential of the whole population increases. Our results imply that both the suppression of recombination and the degeneration of Y chromosome may be associated with reproductive strategy and favoured in polygamous populations with faithless mating partners.

Figure 1

The example genome of an individual in the standard Penna model. The diploid genome is composed of two bitstrings corresponding to chromosomes, in which functional and defective alleles are marked by 0 and 1, respectively. The way of activating genes during the simulation is presented below. In the first year, two alleles in the first locus of the genome are activated. The phenotypic defect is expressed if the both alleles are mutated. In the second year, alleles in the second locus are activated and so on. The number of activated loci determines the age of the individual and increases with the simulation time. In the last year of individual’s life, all genes are active. Each individual can live as long as many bits are present in its chromosome.

Figure 2

The stages of generation of a new individual. (a) Two diploid parental genomes represented by pair of bitstrings, i.e. homologous chromosomes, participate in the generation of a new offspring. (b) The genomes are duplicated to imitate DNA replication process. During this process, a new mutation, marked by an arrow, is introduced with probability M into a randomly chosen bit, i.e. gene, on the replicated chromosomes. (c) Next, during the formation of gametes, the new copies of bitstrings recombine with probability C at the randomly chosen intergenic sites, marked by red dashed lines. (d) The process produces haploid gametes. (e) One of two possible gametes is chosen from each of partner and a diploid zygote is formed.

Figure 3

Modifications of the standard model. (a) A part of lattice with the position of a female seeking for her potential partner in the distance range D_p and putting their child in the distance range D_c. (b) The simplified genome scheme composed of 23 pairs of chromosomes used in the study. One group of genes, called housekeeping, is activated at once since the embryo development. The second smaller group of genes is activated only chronologically during the lifetime of individual.

Figure 4

Fraction of defective alleles in the loci of the 10th autosome or sex chromosomes calculated in all individuals after 1,000,000 MCs. The x axis corresponds to genes ranked according to their activation time; the y axis corresponds to the mean fraction of deleterious alleles for the given gene; b is the time of birth; R is the first year of reproduction. The upper plots concern the simulations with turned on recombination between the X and Y chromosomes. Note, the growing fraction of defective loci activated after the minimum reproductive age. The bottom plots refer to the simulations with turned off recombination between the X and Y chromosomes. Note, the large fraction of defective loci on the Y chromosome independently on the activation time of genes.

Figure 5

Results of computer simulations with unfaithful mating pairs for three assumptions on the recombination between X and Y chromosomes. The left panel (a,c,e) The ratio of the number of mutated alleles in the X chromosome to the 10th autosome (X/10) and in the Y chromosome to the X chromosome (Y/X), calculated for individuals in various age: new-borns, youths and adults. The right panel (b,d,f) The ratio of males to females (M/F) calculated for individuals in various age: new-borns, youths and adults. New-borns are individuals before the birth age; youths are individuals between the birth and reproductive age, and adults are individuals after the reproductive age. Points for the ratio of defective mutations in Y/X (new-borns) and Y/X (youths) as well as for X/10 (new-borns) and X/10 (youths) overlap.

Figure 6

Changes in the recombination rate between the X and Y chromosomes during simulations for two reproductive strategies: unfaithful and faithful mating pairs. Values on the y axis are mean of recombination in a given simulation step divided by the initial value typical of X chromosomes. Three models were considered, with the lattice assuming distance ranges for searching for a partner and putting a child, D_p = 6 and D_c = 6 (a), D_p = 64 and D_c = 64 (b) as well as a model without the lattice (c).

Figure 7

The comparison of the average minimum and maximum values of males to females ratio (M/F) as well as the ratio of the number of mutated alleles in in the X chromosome to the 10th autosome (X/10) and in the Y chromosome to the X chromosome (Y/X) for different simulation scenarios. The average values were calculate for 50 repetitions of simulations in each scenario after 1,000,000 MCs. Various parameters and conditions of the simulations are marked by abbreviations. T is the threshold for the number of defective loci which kill the individual because of the genetic death. The parameters and conditions of simulations: RU - X-Y recombination turned on and unfaithful pairs; T = 3, RF - X-Y recombination turned on and faithful pairs; T = 20, NU - X-Y recombination turned off and unfaithful pairs; T = 3, NF - X-Y recombination turned off and faithful pairs; T = 20, EU - freely evolving X-Y recombination and unfaithful pairs; T = 3, EF - freely evolving X-Y recombination and faithful pairs; T = 20.