“The queen of problems”: the evolutionary paradox of sex

As Ella Fitzgerald sang “birds do it, bees do it, even educated fleas do it”, and turns out the majority of the animal kingdom does it. Do what you ask…well maybe not fall in love as she implied, but most animals do sexually reproduce, with only around 0.1% of animals being known to be exclusively asexual. Yet this predominance of sex has been puzzling biologists for decades leading it to be called 'the queen of problems in evolutionary biology'.  But why is the ubiquity of sex so confusing?

Well, sexual reproduction has many costs compared to asexual reproduction with the main cost of sex being the production of males. Unlike females who directly produce offspring, males typically invest minimally in offspring, often only providing their genetic material. As a result, a population of asexual females should theoretically grow at twice the speed of a sexual population where females waste half their resources on producing males. Sex is therefore often said to have a two-fold cost compared to asexual reproduction.

However, in reality this cost is unlikely to be exactly two-fold. Males may invest more in offspring production for example through providing parental care, which could lower the cost of males. However, the cost of males could also increase due to sexual conflict which arises when the fitness interests of males and females differ. Sexual conflict can result in the evolution traits in males that maximise their reproductive success even if this comes at a cost to females. For example, in seed beetles males have evolved sclerotized spines on their intromittent organs which harm females during copulation. Sexual conflict can therefore increase the cost of sex for females.

But it doesn’t end there. In addition to the cost of males, sex can have even more costs. For example, finding a mate can take a lot of time and energy and can also be risky; there is increased risk of predation and disease transmission, individuals may fail to find a mate or fertilisation may not be successful.

So, given all these costs of sex, why is it still the prevalent mode of reproduction across animals? What are the benefits of sex that can outweigh its many costs?

 The key benefit of sex is thought to be recombination. Recombination occurs during meiosis when homologous chromosomes exchange DNA, creating new combinations of alleles. In the short-term recombination can be thought of as another cost of sex, as it breaks up favourable gene combinations brought together by selection. However, in the long-term, recombination increases the efficiency of selection. Many different theories have been proposed on the exact benefits of recombination, but they can be broadly categorised into ecological and mutation-based models.

Ecological models focus on how the genetic variation recombination generates accelerates the rate of adaption. There are many different ecological hypotheses but the most popular is the Red Queen hypothesis. In the Red Queen hypothesis, parasites attack the most common host genotypes and so the genetic variation sex generates enables escape from these co-evolving parasites. Some evidence for this hypothesis comes from a freshwater snail where the frequency of sex is positively correlated with the frequency of parasite infection. However, there are limitations to this hypothesis. For example, an assumption of the Red Queen hypothesis is that parasites must have severe fitness consequences for the host, which may not always be the case. Furthermore, co-evolving parasites do not select for sex specifically, but instead for genetic diversity. This diversity does not need to be generated by sex but instead could be produced in less costly ways such as the evolution of multiple asexual lineages. This could either from repeated mutation from sexual to asexual reproduction or from mutation within asexual individuals.

A different approach is the mutation-based models which suggest that recombination is advantageous as it prevents the accumulation of deleterious mutations in the genome. If the rate of genetic mutations arising per genome per generation is sufficiently high, this removal of deleterious mutations is predicted to be sufficient to overcome the two-fold cost of sex. However, these models again have restrictive assumptions requiring high mutation rates, large population sizes or particular patterns of epistasis.

A solution to the problems of both these models could lie in an approach termed the pluralistic approach. Rather than viewing these models as competing hypotheses, the pluralistic approach considers how they could act simultaneously and even interact synergistically. Modelling has shown that, in combination, the limitations of the Red Queen and mutation accumulation hypotheses can be overcome, and together they are theoretically sufficient to explain the evolution and maintenance of sex. Despite the pluralistic approach emerging over two decades ago, however, there remains a lack of empirical studies to support the theory, due in part to the difficulty of testing multiple hypotheses together.

So, the paradox of sexual reproduction remains unresolved. While work over the last few decades has produced various interesting hypotheses for the advantages of sex, models inevitably have limitations. More recently, a move towards considering multiple hypotheses acting together is a promising avenue but still lacks sufficient empirical testing. For now, the mystery of sex continues.