February 3rd, 2010
Bioe 109
Winter 2010
Lecture 12
Linkage disequilibrium and the evolution of sex
- there are really only two features that distinguish sexual from asexual reproduction: meiosis and syngamy.
- meiosis is the process by which a diploid organism produces haploid gametes.
- syngamy is the fusion of two haploid gametes to produce a diploid zygote.
- during meiosis, the genes of each parent are “shuffled” such that each gamete, while possessing half of the parental genotype, carries a unique combination of parental genes.
- this “shuffling” arises by recombination which includes two components; independent assortment and crossing-over.
- as a consequence, sexual reproduction is capable of generating a wider variance of phenotypes.
How and why did sex evolve?
- the question of why sex evolved is largely intractable.
- in posing this question, we are really asking about something that happened very early in the history of life on earth.
- in this regard, it resembles questions pertaining to the origin of life on earth.
- in many species sexual reproduction is associated with the evolution of anisogamy.
- anisogamy refers to the presence of large eggs and small sperm.
- phylogenetic evidence clearly shows that anisogamy evolved from isogamous organisms (such as many yeast and algal species) where cells of the same size unite if they belong to different mating types (i.e., + and -).
- again, some theoretical models have explored the conditions under which this may have evolved.
- Charlesworth’s (1978) model has shown that anisogamy can evolve if one genotype (female) is favored because the large size of its gametes enhances the survival of its offspring.
- another genotype can then be favored by virtue of its making many small gametes (male).
- if alleles at a gene controlling gamete size, G, (alleles for small size, S, and large size, L) enters a population in which two alleles already exist at a mating type locus, M, (+ and -), then selection will favor the two loci to become tightly-linked:
- this will create linkage disequilibrium in the population:
M G
______|_|______
+ L
M G
______|_|______
- S
- recombinants formed between these “parental” forms are expected to be less fit (convince yourself that this is the case).
- these linkage groups set the stage for the evolution of sex chromosomes.
What is linkage disequilibrium?
Linkage equilibrium occurs when the genotype present at one locus is independent of the genotype at a second locus.
Linkage disequilibrium occurs when genotypes at the two loci are not independent of another.
What creates linkage disequilibrium?
1. Epistatic natural selection
- epistasis occurs when the fitness of a genotype at one locus depends on its genotype at another locus.
- strong epistasis can create linkage disequilibrium even if the loci are unlinked!
2. Random genetic drift
- this is much less effective than selection in creating disequilibrium.
- sizable disequilibrium can only occur as a consequence of large genetic bottlenecks or founder effects.
- however, in a large population random drift is too weak to cause measurable nonrandom associations of genotypes.
3. Population admixture
- this can be as important at selection in creating disequilibrium.
- the mixing of two differentiated groups will create disequilibrium only if they possess different frequencies of chromosomes (see fig. 7.5 in the textbook).
What eliminates linkage disequilibrium?
1. Recombination!
- recombination will erode linkage disequilibrium quickly is rates of recombination are high.
- if the loci in linkage disequilibrium occur in chromosomal regions experiencing low rates of recombination, the disequilibrium will take a long time to decay.
Why sex?
- given the vast array of possibilities, why do the majority of species reproduce sexually - what are the advantages of sexual reproduction?
- if sex did not have such a large intrinsic advantage, then we would expect to see many more obligate asexual groups
- in fact, they represent only a small fraction of all species (less than 0.01% of all species).
- the phylogenetic distribution of asexual species suggests that they do arise continuously from sexual species.
- almost without exception, asexual species are observed at the tips of phylogenetic trees.
- this suggests that these asexual lineages flourish for relatively short periods of time but typically become extinct long before closely-related sexual groups.
- with the possible exception of the bdelloid rotifers, there have been no major adaptive radiations of asexual groups.
- in other words, asexual lineages have not been a major contributors to macroevolution.
- is this a problem?
- in fact, it is a problem because we realize that sex confers a number of important “costs” as well as benefits.
- what are these “costs” of sex?
The costs of sex
1. The cost of producing males
- the first of these “costs” is that of producing males (this is also called the “two-fold cost of sex”).
- consider a female of a sexual species having an equal sex ratio.
- when she reproduces, she allocates 50% of her genes to each of her progeny - the other half obviously contributed by the father.
- if she abandoned sex and reproduced parthenogenetically, she would forego the production of sons and only produce daughters.
- these daughters would mature and reproduce parthenogenetically as well.
- very rapidly, the population would be taken over by females who reproduce by parthenogenesis.
2. The costs of finding mates
- if population density is low individuals of both sexes may not actually be able to find a mate.
- in extreme cases, in which a single individual has dispersed a great distance - say onto a remote island group - it is out of luck (unless it can self).
3. The costs of mating
- another cost occurs because mating is an extremely risky business for many species.
- in addition to expending considerable resources for mating, courtship displays commonly render individual males vulnerable to predation.
- finally, sexual reproduction creates opportunities for sexually-transmitted diseases.
- asexual populations simply do not face these problems - time and energy are saved.
3. The cost of recombination
- recombination not only leads to the production of unique gene combinations, it also breaks them apart.
- therefore, genotypes with unique combinations of genes favored in one generation in one particular environment will not be conserved in the next generation.
- this may be viewed as a cost but must obviously be weighed against the benefits provided by recombination.
- a number of advantages to sexual reproduction have been proposed.
- here are the three most likely advantages:
1. Adaptive evolution is enhanced.
- this is the classic argument favoring sexual reproduction.
- for two advantageous mutations to occur in the same asexually-reproducing individual, they must sequentially.
- this is expected to occur very rarely and very slowly.
- in contrast, with recombination it is easy to produce a genotype that possesses two or more advantageous mutations.
- this can greatly accelerate the rate of adaptive evolution.
- therefore, adaptive evolution can occur much more rapidly in sexual populations.
2. The Red Queen hypothesis
- the name of this hypothesis comes from Lewis Carroll’s novel “Through the looking glass”.
- Alice and the Red Queen find themselves running across a chessboard but don’t seem to be moving anywhere.
- similarly, species populations are viewed as having to continuously “run” (read evolve) to track changing environments just to keep even.
- if they fail to adapt to the changing conditions, they are liable to go extinct.
- in addition to changing abiotic conditions, the biotic environment is always going to be changing.
- predators are becoming better predators, competitors are becoming better competitors, parasites are becoming better parasites.
- if a species does not continuously keep up it is likely to be displaced by a competing species.
- this is where the advantage to sexual reproduction is believed to lie.
- sexually reproducing populations, by virtue of their enhanced ability to generate variation quickly, are able to track changing environments more effectively than asexual species.
3. Muller’s ratchet
- this one of the most influential arguments favoring sexual reproduction.
- it addresses the ability of sexual and asexual populations to deal with harmful deleterious mutations.
- consider an sexual population with a quasi-normal distribution of mildly deleterious mutations.
- the most fit individuals possess the lowest number of mildly deleterious mutations, but this group is unlikely to be the most frequent.
- by chance, this group has the possibility of going extinct by random drift.
- when this happens, the fittest genotype has been lost - “Muller’s ratchet” has made another turn.
- now the most fit group is that that has one more deleterious mutation than before - the “mutational load” has increased.
- there is only one direction for asexual populations to move - towards ever greater loads of deleterious genes.
- as this process continues, asexual populations are expected to gradually decline in fitness and when placed in competition with sexual populations will lose out.
- sexual reproduction breaks the ratchet.
- when the least mutated class in a sexual population is lost be drift, recombination can recreate the lost mutational class having the highest fitness.
- in addition to purging deleterious mutations, advantageous mutations that drive progressive evolution have a better chance of being decoupled from deleterious genetic backgrounds in sexual than asexual populations.
- the same mutation entering a sexual population in one genetic background is not constrained to persist in that background.
- in fact, it will be recombined into a diversity of different genetic backgrounds - the mean fitness of that advantageous mutation will averaged over all genetic backgrounds.
- as a consequence, sexual populations will enjoy a higher rate of adaptive evolution.
Q: Why then do asexual species only occur on the tips of phylogenetic trees?
A: Because of the short term advantages of asexual reproduction lose out to the long-term benefits of sexual reproduction.