Why is sexual reproduction so common in nature?

Many theoretical models have been developed to show the conditions under which there is a sufficiently large short-term advantage for sex to offset this two-fold cost.  The general consensus amongst evolutionary biologists is that there are two relatively convincing, modern day theories.  Both of these theories are concerned with a deterministic advantage to sex and recombination through the production of genetically variable offspring.  This increases efficiency of selection, and hence accelerates the increase in mean fitness.

The first of the two theories is known as the Mutational Deterministic Hypothesis (Kondrashov, 1988), and states that sexual reproduction can enable females to reduce the number of deleterious mutations in their offspring.  This idea requires that each deleterious mutation leads to a greater decrease in log fitness than the previous mutation (synergistic epistasis between deleterious mutations).  The principle theme is that when this is the case, sexual reproduction increases the variance in the number of mutations that will be carried by the offspring.  The subsequent lowered fitness of the individuals carrying above average numbers of such deleterious mutations will lead to an increased number of deleterious mutations being eliminated from the population.  If the resultant mutation rate per generation is sufficiently high, then this process can theoretically fully compensate for the two-fold cost of sex.

However, the genomic mutation rate (U) is exactly where the problem lies, as the plausibility of such a theory is dependent upon a relatively high rate of mutation within the genome.  A female gains the advantage whatever the deleterious mutation rate, but the relative benefit increases with the mutation rate.  But what deleterious mutation rate is needed to outweigh the two-fold cost of sex?  Kondrashov suggests that the answer depends essentially on the details of the theoretical model, but a rate of about one new deleterious mutation per individual is probably sufficient.  Thus, sex becomes advantageous relative to cloning if U is more than about one.  This is the most controversial point in this theory, because deleterious mutation rates have historically been thought to be much lower.  Mukai has performed a number of experiments on Drosophila and deduced that a mutation rate of 0.5 per individual per generation was sufficient.  The problem concerning mutation rates is difficult to solve as there is no strong factual evidence that exists to rule out mutation rates as high as are required for sex to prosper.  However, Mukai’s estimate of 0.5 per individual was a lower bound estimate, and his results are also compatible with a figure greater than one.

The second of the two modern day models ignores the effect of deleterious mutations and concentrates on external environmental change.  This model suggests that sex accelerates adaptation to a changing environment by creating new gene combinations.  The problem is to work out how environments could possibly change fast enough, ie: at a rate that makes sex beneficial every generation.  Currently, the most interesting and promising hypothesis – the Red Queen – suggests that coevolution between hosts and parasites may generate environmental change at a rate that renders sex advantageous in the long term (the ‘environment’ for the parasite is the host’s resistance mechanism, and the ‘environment’ for the host is the parasite’s penetration mechanism).  Usually parasites are assumed to provide the antagonistic driving force in this co-evolutionary dance, though host immune systems may laso do so.  The dance is a consequence of time lagged selection by co-evolving parasites against common host genotypes, leading ultimately to sustained oscillations in host and gene frequencies.

Substantial evidence has been provided to support the Red Queen Hypothesis, which is why it stands as one of the more convincing theories explaining the evolution of sex.  For example, Baer et al. wrote a paper on how experimental variation in polyandry affects parasite loads and fitness in a bumble bee.  Through artificially inseminating queens of a bumble bee with sperm of either high or low genetic diversity, they tested the hypothesis that genetic diversity among a female’s offspring may offer some protection from parasitism.  The results they obtained conclusively revealed that colonies of high diversity had fewer parasites and showed greater reproductive success on average – thus emphasising that sex may have evolved to provide sufficient genetic variation to cope with the ever present onslaught of parasites.

So far, two modern day theories have been discussed in an attempt to justify why sexual reproduction has evolved and why it is so common.  However, is it correct to assume that the prominence of sex across the natural word can be ultimately explained by either one hypothesis or the other?  According to West, Lively and Read♣, looking at the theories in isolation is ineffectual, and instead they suggest looking at the advantages that may be gained from using a pluralistic approach to consider and test models of sexual reproduction.  

West et al. argue that the pluralistic approach should be considered as it is entirely plausible that multiple mechanisms may be providing an overriding advantage to sex, and/or that the different mechanisms may be important in different species or environments.  That is, multiple selection pressures may be at work.  Secondly, West et al. argue that more than one mechanism may be required to fully balance the two-fold cost of sex.  When looking at the mechanisms individually, extreme assumptions are required in order to completely explain the maintenance of sex; however, if the two mechanisms are considered simultaneously, the assumptions can be relaxed.  Finally, the paper quite importantly contends that different mechanisms may not only interact simultaneously, but also synergistically.  Given such interactions, the maintenance of sex can be explained with much more reasonable and less extreme assumptions than each of the theories acting alone.

But in what combination are the Red Queen (RQ) hypothesis and Mutational Deterministic (MD) hypothesis most likely to be found and considered effective?  Does the RQ theory aid the MD hypothesis, or visa versa?  There are advantages for both possible combinations as environmental and mutational mechanisms complement each other and help compensate for each others weaknesses.  Such relations imply that the resultant combined effects of both mechanisms are likely to be more advantageous than the sum of their parts.

One of the main problems with the RQ hypothesis is that it requires that parasites have a severe detrimental effect on the host fitness, or alternatively, only the fittest hosts will survive to reproductive maturity.  The MD hypothesis was put forward to compensate for these problems in a simulation model constructed by Howard and Lively (1994), where both parasite-host interactions and mutation accumulation were allowed to occur simultaneously.  The results form the model showed that the outcome of deleterious mutations were multiplicative and therefore showed that the MD process was not operating.  Instead, gain in mutations was taking place through Muller’s ratchet – the ‘irreversible decrease in fitness that can occur through the stochastic accumulation of deleterious mutations in finite sexual populations’.  Acting alone, Muller’s ratchet was shown to operate too slowly to provide a significant short-term benefit to sex.

The simulation model demonstrated that the moderate effects of parasites in combination with a reasonable mutation accumulation rate could more than balance the two fold cost of sex – but how exactly?  In the short term, parasites effectively prevented the fixation of clones and thus the elimination of sex.  In the long term, mutation accumulation led to the eventual extinction of clones.  The extinction occurred because mutations in clonal lineages are enormously aided by parasite-driven oscillations, primarily because rate of mutation accumulation is enhanced during periods in which the clone is driven to low numbers by the parasite.

The alternative combination is that the environmental RQ hypothesis aids the MD process.  The problem with the MD hypothesis is that high rates of deleterious mutations are required, often greater than one mutation/genome/generation.  Most of the models used to describe the MD process often assume infinite populations often assume infinite populations and consider populations at equilibrium in mutation-selection balance, bypassing the fundamental dynamics required to reach this situation.  The RQ hypothesis can be manipulated to solve such dilemmas, as it produces frequency-dependent selection and so slows down the spread of asexual clones, allowing more time for mutation-selection balance to attained.  West et al. then go on to argue that the RQ hypothesis reduces the fitness advantage of asexuals, reducing the number of deleterious mutations that are needed to reduce the asexual fitness below that of sexual individuals.  Furthermore, it may even increase the rate at which an asexual line accumulates mutations (through stochastic process of Muller’s ratchet), leading to an increased reduction in fitness and therefore allowing mutation-selection balance to be reached more efficiently.

The idea put forward by West et al. is important in attempting to explain the problem that although deleterious mutations and parasite-host coevolution are reasonable theories, it still has not been conclusively shown that either really explains how sex is maintained in nature.  However, further tests still need to be carried out on the pluralistic approach, meaning that sex still persists as a puzzle for evolutionary biologists.