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Good genes do not always lead to evolutionary success

The theory of sexual selection proposes that, where males have to compete to mate with females, the males may develop indicators of “good genes,” in order to impress and gain access to females. Indicators may include things such as large body size, impressive horns or feathers, or the ability to win physical fights. In theory, the males with the best genes will sire more offspring and thereby their impressive traits will spread within the population, leading to increased success for all. 

Past field studies have sometimes shown that this is not how it works in nature. In fact, males can sometimes go to extremes to demonstrate their fitness and this may impact females negatively and lead to less successful reproduction for them. In the end, with fewer offspring being born to the females, recruitment into the population may diminish to the extent that the population may even collapse completely. 

Scientists from Imperial College London and the University of Lausanne have now developed a model that explains how so-called “good genes” in males can sometimes be disadvantageous for females and, indeed, for an entire population. The model, published in the Proceedings of the National Academy of
, tested theories of sexual competition and compared the results with data from various population experiments, in order to provide a possible explanation for why sexual selection can improve male condition while, at the same time, being disadvantageous for female fitness and population viability.

“Where males evolve selfish traits that help them individually win, they can actually end up causing the population to crash – it’s a form of evolutionary suicide. Even when females evolve to counter male harm and prevent population collapse, the population still decreases significantly, reducing its viability,” said study first author Dr. Ewan Flintham.

A prime example of this is the phenomenon of infanticide in lion prides. Dominant males may kill offspring sired by other males, leading to lower reproductive rate for females and, potentially, lower recruitment into lion populations. Other examples include the mating practice of male bed bugs that inseminate females by piercing holes directly into the body cavity, courting antelope that chase and harass females to the point of exhaustion, and brawling male elephant seals that trample pups to death while defending a harem of females.

The team’s model considered different scenarios where individuals vary in their condition. Good condition is considered to be evidence of good genes, but male animals in good condition will experience more intense sexual conflict as they compete more for access to females. If this competition has the effect of harming females, it may well end up backfiring and generating a negative association between male condition and population size. 

The new model provides an explanation for why some experiments show male condition improving, without female fitness or population viability improving alongside. This occurs because sexual selection favors genes that improve condition, which can then lead to more sexual conflict and more significant harm to females. Population decline or crash can result from this situation, according to the predictions of the model. This finding contrasts with the common view that sexual selection on good genes also improves mean fitness of the population.

Sexual interactions like these are an important component of understanding population demographics and conservation. For example, where there are more males, sexual competition intensifies, meaning harm towards females is more likely. This is also true in human-managed populations, for example domestic carp, where males and females must be isolated during spawning season.

Dr. Flintham completed the study as part of his research at the Centre for Doctoral Training in Quantitative and Modelling Skills in Ecology and Evolution at Imperial. His project supervisor and study co-author was Professor Vincent Savolainen, director of the Georgina Mace Centre for the Living Planet at Imperial.

“Male harm evolved in nature as something that was supposed to be good, but is detrimental to females and the whole population. Questions like how and why this happens can only be answered with quantitative methods – data and mathematical models – which can be just as important as field studies,” said Savolainen.

By Alison Bosman, Staff Writer

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