Fruit flies are tiny insects that are often found near rotting fruits and vegetables. They are also widely used as model organisms for studying sexual selection and evolution.

But what do female fruit flies look for in a mate? Do they prefer males with the best genes, or males whose genes match their own? And how do they ensure that their offspring have the highest fitness possible?

Genetic Quality vs Genetic Compatibility
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Researchers at the University of Zurich and Concordia University have investigated these questions by staging competitive matings of fruit flies.

The male competitors differed in the quality of their genes and in their genetic compatibility with the target female.

The researchers used fluorescently labeled sperm to track the entire reproductive process, from sperm in the female reproductive tract to paternity outcomes.

They found that both factors - genetic quality and genetic compatibility - influence reproduction, though varying in importance across reproductive stages.

For example, males with high-quality genes generally have higher mating success.

This means that they are more likely to mate with females and transfer more sperm to them. High-quality genes can enhance the survival, growth and reproduction of the offspring.

However, females, who routinely mate with multiple males, can influence sperm storage and fertilization success by ejecting some of the sperm after mating.

This is a way for females to adjust their mate choice after copulation.

Females appear to delay this sperm ejection if a male has better genes or is more compatible with the female than his predecessor.

This gives the preferred sperm more time to enter the female storage organs and displace the rival sperm already residing there. The complex interplay of these processes ultimately affects paternity.

Why Does Genetic Compatibility Matter?

Genetic compatibility refers to how well the genes of two individuals match or complement each other. This can affect the fitness of the offspring in various ways.

For example, some genes may have positive effects when present in a single copy (heterozygous), but negative effects when present in two copies (homozygous).

This is called overdominance or heterozygote advantage. In this case, mating with a genetically dissimilar partner can increase the chances of producing heterozygous offspring with higher fitness.

Another example is when two individuals carry different variants of a gene that interact with each other to produce a beneficial outcome. This is called epistasis or gene-gene interaction.

In this case, mating with a genetically similar partner can increase the chances of producing offspring with optimal gene combinations.

Genetic compatibility can also affect the immune system of the offspring. Some genes encode for proteins that recognize and fight against pathogens.

These genes are called major histocompatibility complex (MHC) genes.

Mating with a partner who has different MHC genes can increase the diversity of the offspring's immune system and make them more resistant to infections.

How Do Female Fruit Flies Optimize Their Offspring's Fitness?

The researchers suggested that female fruit flies use different criteria across stages of the reproductive process to influence the outcome of their mating activity.

They proposed that females first select males based on their genetic quality, which can be assessed by their physical traits, such as body size, color and courtship behavior.

Then, they fine-tuned their choice based on their genetic compatibility, which can be assessed by chemical cues, such as pheromones and seminal fluid proteins.

By doing so, females can optimize the fitness of their offspring by maximizing both genetic quality and genetic compatibility.

This is a sophisticated interplay between pre- and post-copulatory mate choice mechanisms that can shape the evolution of male sexual characteristics and population variation.