Male aggression is a threat to the survival of species

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Sexual conflict in the elegant bark beetle (Ischnura elegans): males squeeze fem
Sexual conflict in the elegant bark beetle (Ischnura elegans): males squeeze females tightly using the tips of their abdomens (left panel) until they accept them as mates. Such pre-copulatory behavior carries costs for both sexes, including physical damage (see the damaged wings on the right panel) or increased risk of predation, thus generating a form of sexual conflict. © Erik Svensson - Lund University, Sweden
A fan-shaped tail with shimmering colors in the peacock, eyes perched at the ends of long stems on either side of the head in the Diopsidae flies. The different finery that males use to distinguish themselves is the "seductive" part of mating. The aggressiveness they show to each other, and especially to females, can have an extremely deleterious effect on the biology of populations. This could potentially lead to extinction, according to a study by the Department of Ecology and Evolution of the University of Lausanne, published on 27 February 2023 in the journal "PNAS".

Sexual selection is at the heart of evolutionary biology with two theories to explain two types of traits. On the one hand, the so-called ’handicap principle’: in order to allow females to evaluate the quality of their potential partner, males will try to differentiate themselves by means of distinctive signals, such as elaborate dances in birds of paradise, a hoarse and noisy song in frogs or conspicuous tubercles in roaches. However, these exaggerated sexual characteristics are very costly (the peacock’s imposing tail and the fly’s perched eyes impede flight) and, through their exuberance, may attract predators. To females, however, these signals are a sign of good genetic health, as the breeder manages to survive despite a severe handicap. By selecting the most attractive males, they ’purge’ the bad mutations.

The other strategy put in place to ensure offspring is the sexual conflict theory. This involves aggressive interactions with females to force them to mate, often at the cost of their fertility and sometimes even their lives. In the bed bug, for example, males tear the abdomen of females to insert their sperm directly into it, which causes wounds that are difficult to heal and leads to the danger of infection. In the vinegar fly, it is the seminal fluid that contains toxic proteins that prevent the females from mating again, at the cost of their future fertility.

The classical hypothesis question ed

What happens when these two theories intersect? In other words, when males in better condition can develop more aggressive traits that allow them to mate more often, but at a higher cost to the females? Our findings run counter to the classical hypothesis that sexual selection promotes healthy populations by eliminating ’bad genes’," says Charles Mullon, assistant professor in the Department ofEcology and Evolution (DEE) of the Faculty of Biology and Medicine of the University of Lausanne and director of the study published on 27 February 2023 in the journal Proceedings of the National Academy of Sciences (PNAS). ’We show, a contrario, that competition to fertilize the maximum number of females can have a strongly deleterious effect on population biology, potentially leading to extinction, while paradoxically increasing genetic quality.’

Indeed, by developing traits that improve their mating success, healthier males, especially with ’better genes’, harm the females and, in so doing, jeopardize the survival of the species that depends on the fertility of the latter. An example of this is the case of the vinegar fly: larger and stronger males, because they are better fed, are more aggressive towards females and have a more deleterious impact on their fellow males than those in less good condition.

The effect of good genes becomes detrimental

The ’good gene’ hypothesis is thus undermined. It postulates that sexual selection on condition-dependent traits indirectly increases the average condition and thus the health of the population. Researchers from the University of Lausanne, in collaboration with the Department of Life Sciences of Imperial College London, demonstrate with the help of mathematical models that such an effect is rarely to be expected when sexual traits cause damage.

We have developed models of the evolution of sexual conflict where individuals vary in condition. We show that conflict is more intense in populations where members are in better condition, for example because they are better nourished or carry fewer deleterious genes. Such intensified conflict reduces female fertility, which can potentially lead to extinction. More generally, there is a negative association between better condition and population size, which is counterintuitive. The supposedly beneficial outcome of good genes is therefore actually more damaging to populations’, says Ewan O Flintham , first author of the study and first assistant in the DEE after a PhD thesis in the Department of Life Sciences at Imperial College London. The team’s mathematical models show that it doesn’t take much to see this damage. It may be enough, for example, for one male to reduce the fertility of one female by 2% per interaction for the population size to almost halve.

Towards new fields of research

Based on these results, the Lausanne group proposes to analyze in new research whether condition-dependent trait expression has an effect not only on sexual competition, but also on competition for other resources and on social interactions.