Explaining the evolution of sex and recombination

Transcription

1 Explaining the evolution of sex and recombination Peter Keightley Institute of Evolutionary Biology University of Edinburgh

2 Sexual reproduction is ubiquitous in eukaryotes Syngamy Meiosis with recombination

3 Sex and recombination have potential disadvantages Meiotic recombination breaks apart combinations of genes that have been built up by selection.

4 Sex and recombination have potential disadvantages Meiotic recombination breaks apart combinations of genes that have been built up by selection. Sexual reproduction requires finding a mate, which carries risks.

5 Sex and recombination have potential disadvantages Meiotic recombination breaks apart combinations of genes that have been built up by selection. Sexual reproduction requires finding a mate, which carries risks. Sex can carry a two-fold cost if population growth is limited by the number of females.

6 Why are sex and recombination almost ubiquitous in nature?

7 Why are sex and recombination almost ubiquitous in nature? Why don t asexuals take over sexual populations?

8 Is there a general explanation for the evolution of recombination? Collaborator: Sally Otto University of British Columbia

9 Association between beneficial (+) and deleterious alleles (-) Four chromosomes in a population

10 Association between beneficial (+) and deleterious alleles (-) Alleles at the loci are negatively associated. The coupling types ++ and -- are absent.

11 Association between beneficial (+) and deleterious alleles (-) Alleles at the loci are negatively associated. The coupling types ++ and -- are absent. The effectiveness of selection acting on variation at the loci is weakened.

12 Mutations that increase recombination are favoured if there are negative allelic associations m m m m

13 Mutations that increase recombination are favoured if there are negative allelic associations M m m m

14 Mutations that increase recombination are favoured if there are negative allelic associations M m m m + + M A mutation (M) at a linked locus that increases recombination is favoured because it hitchhikes on chromosomes carrying multiple beneficial alleles, generated by recombination. Felsenstein & Yokoyama 1976

15 Non-random associations between linked loci arise in two ways 1. Directional selection. + + size is very large Rapidly fixed Rapidly eliminated

16 Non-random associations between linked loci arise in two ways 1. Directional selection. size is very large

17 Non-random associations between linked loci arise in two ways 1. Directional selection. size is very large BUT non-random associations are expected to be absent in large populations if there is some recombination. Disequilibrium Pop. size

18 Non-random associations between linked loci arise in two ways 2. Synergistic epistatic interactions between loci Unfit combination that is rapidly eliminated

19 Non-random associations between linked loci arise in two ways 2. Synergistic epistatic interactions between loci BUT there is little empirical evidence for this kind of epistasis.

20 Is recombination favoured in the presence of selection at multiple linked loci?

21 Simulating the fate of a recombination modifier in the presence of selection and mutation at multiple linked loci Population of N haploid individuals at equilibrium between linked deleterious mutations and selection.

22 Simulating the fate of a recombination modifier in the presence of selection and mutation at multiple linked loci M Introduce a mutation that increases recombination. Frequency = 1/N

23 Possible fate of a recombination modifier mutation Modifier lost M

24 Possible fate of a recombination modifier mutation Modifier lost M M M M M M M M M M M M M M M M M M M M M M M MM Modifier fixed Happens at a frequency of 1/N by chance

25 Modifiers mutations that increase recombination were always observed to be favoured

26 Recombination is strongly favoured in nonrecombining systems Relative fixation rate of modifier Recombination modifier increasing map length by 0.1M Initial recombination rate (map length, L)

27 The advantage of recombination increases with population size Relative fixation rate of modifier Map length L = 0 L = 0.1 L = Population size, N

28 The advantage of recombination increases with population size Relative fixation rate of modifier Map length L = 0 L = 0.1 L = Population size, N This property emerges because of the multi-locus nature of the model. In systems with small numbers of loci, recombination is favoured only in small populations.

29 Why does the advantage of a recombination modifier increase with population size? Selection generates multi-locus associations.

30 Why does the advantage of a recombination modifier increase with population size? Selection generates multi-locus associations. Large populations maintain more polymorphic loci, and more negative associations, increasing the hitchhiking effect favouring recombination modifier mutations.

31 Why does the advantage of a recombination modifier increase with population size? Selection generates multi-locus associations. Large populations maintain more polymorphic loci, and more negative associations, increasing the hitchhiking effect favouring recombination modifier mutations. The infinite population prediction that negative associations should be absent does not apply when there are multiple loci under selection.

32 Summary Simple simulations show that interference between selected mutations favours mutations that increase recombination.

33 Summary Simple simulations show that interference between selected mutations favours mutations that increase recombination. Theory developed for two- or three-locus systems proved to be misleading.

34 Summary Simple simulations show that interference between selected mutations favours mutations that increase recombination. Theory developed for two- or three-locus systems proved to be misleading. The mechanism described is likely to be the general explanation for the evolution of recombination. Mutations affecting fitness are universal and natural populations tend to be very large.