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The Battle of the Sexes:
Sexually Antagonistic Genes in Small Populations

ClaireAsher18 July 2013

By definition, males and females are physically different. In some cases, these differences are restricted to the sex organs, but in many species males and females also differ in their physical appearance and behaviour. What makes you a good male does not necessarily make you a good female, and the benefit of some genes depends upon which sex they find themselves in. These antagonistic genes have sex-dependent fitness effects, and can be a source of genetic variation in natural populations. Research in GEE shows that in small populations, chance events can alter the frequency of antagonistic mutations, and alter the balance of fitness between the sexes. Small populations tend to produce either good males and poor females, or good females and poor males, but not both. This phenomenon could have interesting implications for dispersal and fitness, especially in fragmented populations.

Differences in physical appearance between the sexes is known as sexual dimorphism, and occurs because characteristics that make you good at being male are often different from the characteristics that make you good at being female. A brightly coloured male may get more females because he is more visible or attractive, but a brightly coloured female doesn’t lay more eggs, she just gets eaten.

Sexual dimorphism allows males and females to independently adapt to different optima. The problem is dimorphism is actually quite hard to achieve. Males and females of the same species share, more or less, the same genome. Some species, such as birds and mammals, have sex-specific genes and chromosomes (e.g. the Y chromosome), but these represent a very small proportion of their genes, and many species achieve sexual dimorphism without any sex chromosomes at all. For the most part, traits that differ between males and females are generated from the same set of genes. The evolution of dimorphic traits such as body size, plumage colour and antlers proceeds not through changes to gene function, but changes in gene expression.

Gene Expression and Sexual Dimorphism

Male and female Red Deer
(Cervus elaphus)

A gene that codes for a trait that is beneficial to males but detrimental to females can become sexually dimorphic if it is expressed only when it appears in males (or vice versa). This same gene, when it finds itself in a female body, simply isn’t expressed and does not exert its effect. So a female red deer carries the gene for antlers, but never grows any because the gene is silent.

Sex-specific gene expression is an elegant solution to the problem that males and females face different challenges in life. However, the road to sexual dimorphism is not that straight forward. For a new sexually dimorphic trait to evolve, it must first appear as a novel mutation in a pre-existing gene. At first, it will be expressed just like most other genes – equally in both males and females. This mutation might do great when it finds itself in a male, allowing him to produce more offspring, but when it appears in a female, it would be harmful, reducing the number of offspring produced. For this new mutation to be successful and spread through the population, it needs to avoid the negative fitness effects that come from being expressed in a female. At this stage, a second mutation altering gene regulation – so that the gene is expressed only in males – would be hugely beneficial, but this mutation may take time to arise by chance.

There are many examples in nature of sexually dimorphic traits – genetic variants expressed in one sex but not another. But scientists are increasingly finding mutations that haven’t made it to this happy equilibrium yet – their fitness effect is sex-dependent but they are still expressed in both males and females. These genes are known as ‘sexually antagonistic’ and are thought to be a major source of genetic variation within populations.

Generating Variability
Normally, a gene that has a detrimental effect (i.e. reduces how many offspring you produce) is quickly removed from the population by natural selection. Sexually antagonistic genes are different because their detrimental effect is only seen by natural selection when the mutation appears in one sex. Half the time, the mutation is beneficial, and half the time it is harmful. Overall, the effect of the gene can even out to be essentially neutral. Neutral mutations can stick around in a population for ages, although they may be lost, or spread, by chance.

Chance, also known as genetic drift, can change the frequency of mutations in a population irrespective of their fitness effects, and the effect of chance is much greater in smaller populations. Sexually antagonistic genes may be particularly susceptible to genetic drift because their effect is, on average, neutral. Most theoretical and empirical studies of sexual antagonism use very large populations with high genetic diversity, where the influence of genetic drift is very small. Researchers in GEE have been investigating the evolution of sexual antagonism in small populations to see how chance might influence their frequency.

The fruit fly,
Drosophila melanogaster

The Role of Chance
In a recent paper in Evolution, Jack Hesketh, Kevin Fowler and Max Reuter from GEE looked at how small populations of the fruit fly Drosophila melanogaster evolved, and how sex-specific fitness changed under the influence of genetic drift, through the random spread of sexually antagonistic genes. Four populations of 100 flies were maintained for 80 generations, and the fitness of both larvae and adults was measured in terms of survival (larvae), fertilisation success (males) and egg-laying (females).

Over 80 generations of evolution in the lab, the four fruit fly populations diverged in terms of fitness. Average fitness across the sexes didn’t differ significantly between populations, but there was a strong interaction between population and sex – some populations produced very fit females and unfit males whilst others produced fit males and unfit females. This effect was not present for larval fitness however, which makes sense since larvae are primarily concerned with growth and not reproduction. In the original source populations, some individuals carried mutations beneficial to females, whilst others carried mutations beneficial to males. In this experiment, through the process of genetic drift, different populations ended up with a different selection of these mutations – some populations kept hold of the genetic variants favourable to females and consequently produce very fit females but relatively crap males (and vice versa).

This study shows that in real populations, genetic drift may lead to population-divergence in sexually antagonistic genes. This could have interesting repercussions for fragmented populations where different fragments may diverge differently in terms of sexual antagonism. Dispersal in this situation could be extremely favourable – a fit male in a population full of fit males would be faced with stiff competition, but if he wandered over into a neighbouring population full of unfit males, he would presumably have his pick of the ladies. Max Reuter and colleagues in GEE hope to continue to investigate this phenomenon and its consequences in natural populations.

Original Article:

This research was made possible by funding from the Natural Environment Research Council (NERC) and the Biotechnology and Biological Sciences Research Council (BBSRC).