Suppose we want to test the hypothesis that females choose particular males so they will have more attractive offspring. Verifying that hypothesis would require mate choice trials showing that particular males get chosen more often, and then repeating those trials with the offspring. Researchers often simplify the matter by choosing some proxy of attractiveness like a particular trait — the size of an ornament, for example — and look for correlations in that trait between sires and sons. If we don’t find that sons inherit their father’s trait then can we conclude that the trait does not signal male genetic quality? What if we could show that attractive fathers tend to have attractive sons regardless of their trait sizes? This way we’re letting female insects, rather than male or female primates, tell us who’s an attractive insect.
A recent study by Fiona Ingleby from University of Exeter used fruit flies (Drosophila simulans) to address whether a particular sexual signal was reliable as an indicator of heritable male attractiveness. Several studies have shown that cuticular hydrocarbons (CHCs) affect mate choice in fruit flies. CHCs are volatile chemicals given off by the “skin” of a fly that may act as pheromones. Ingleby and her colleagues John Hunt and David Hosken were particularly interested to see how environmental variation would affect CHCs and mate choice. They also wanted to see if there was a genotype-by-environment interaction (abbreviated “GxE“): the genotype and the environment the flies grow up in could both affect their phenotpyes (CHC production). Would males be attractive in all environments, or would they be attractive in some environments, and unattractive in others?
Ingleby captured flies in Greece, then after a few generations of laboratory domestication raised their offspring in the lab on two different types of food (oats and soy) and at two different temperatures (23C versus 25C). Her paper stresses that these four environments were not that different from each other, and not extreme, and yet they found fairly dramatic variation in phenotypes depending on the environment. Cuticular hydrocarbon (CHC) signal varied across environments, but the researchers found very strong genetic effects on attractiveness across all the environments. Sons tended to resemble their fathers in attractiveness regardless of environment. However, Ingleby, Hunt and Hosken concluded that CHCs are not a reliable indicator of male attractiveness, since the CHC phenotype changed so much across the tested environments.
The researchers considered a few alternative hypotheses to explain this apparent discrepancy: multiple traits, direct benefits and the possibility that other traits account for variation in attractiveness. Perhaps females use not just CHCs but also many other males traits and behaviors when selecting a mate. Females might be able to tell which males’ semen will be less harmful, or more beneficial. This would benefit females directly, instead of just her offspring. Also, the researchers point out, some aspects of CHC profile were reliable indicators of male genotype, and so females are probably using just some CHCs along with other traits to assess males.
The aspect of this study I find most intriguing is showing the heritability of attractiveness, instead of focusing on an arbitrarily chosen trait. Whenever a researcher hypothesizes about a trait being under selection, he hast to make a huge set of assumptions that can only be verified after painstaking data collection that may take decades. Most Ph.D. dissertations are done in less than ten years. Even if a researcher could make a pretty good guess about what traits should correlate with fitness, she would have to have really good luck in finding or creating environmental conditions that would provide good control over that trait. By the time that laboratory-level control is attained, we may have lost touch with the reality of how species live in the wild. Then an experiment might provide a good case study, but it tells us little about the actual evolution of a species. I hope to see more empirical studies that use attractiveness rather than arbitrarily selected characters.
Related articles
- Sexual selection with age-dependent mutation (lxmx.wordpress.com)
- Are humans monogamous? (theratchet.ca)
- Males’ superior spatial ability likely is not an evolutionary adaptation (esciencenews.com)
Sexual Selection and Life History Evolution 
I am compelled to point out some thoughts about this item:
Sexual selection and sexual attraction seem be based on beauty rather than utility, and explains the common observation in nature that it is the most beautiful that survive. Im going to try to explain this. There is a dynamic interaction between the mean number of new deleterious mutations per generation (Mg), the mean number of deleterious mutations in the genome of the population (Mp) and percentage zygote survival (Z). Increased Mg leads to increased Mp and a fall in Zs but it takes several generations before a new equilibrium is reached. If sexual attraction is influenced by the number of deleterious mutations in the genome of individuals then Mp is reduced and Zs increased for any given value of Mg. This fall in Y and rise in Z is more marked in polygamous than monogamous mating systems. And deleterious mutations can occur without any observable or measurable effect on function. Thus sexual selection, in this organism, for low levels of deleterious mutations cannot be based on assessment of performance. Instead it is based on a simple symmetrical surface pattern that is flawlessly reproduced by organisms with no deleterious mutations, but is less than perfect, and therefore less attractive, if genetic systems have been deleted. A complex vital task requires a system with a high level of redundancy that acts so that the loss of one component has no observable effect and therefore cannot be used for sexual selection. The reproduction of a beautiful surface pattern also requires a low error, high redundancy genetic system; however, in this case there is advantage if a single deleterious mutation produces a recognisable change.
Furthermore deleterious mutations interact synergistically causing impaired performance in individual systems and this leads to a positive correlation between the total number of deleterious mutations in the genome and impaired performance across the whole spectrum of biological capability. This includes performance in intellectual tasks, sporting ability, the ability to fight disease and preserve health and the development of a symmetrical physical form. Sexual reproduction distributes deleterious mutations unequally amongst zygotes and Z will correlate negatively with zygote mutational load. Rising environmental mutagenesis will lead to a rise in the human genomic mutational load and to decrease Z, although the full effect would take several generations. So that a marked rise in environmental mutagenesis would lead to species extinction if mate choice were random, i.e., unrelated to the genomic mutational load. The biological imperfections caused by mutations, however, in health, intelligence and physical symmetry are all, to varying degrees, related to sexual attraction. Thefore if mates are chosen in response to sexual attraction the species can be maintained in the presence of high environmental mutagenesis.
Will you say more about the most beautiful surviving? Do you know of evidence for this, or are you going on a general principle?
Darwin’s conception of sexual selection, the one that most biologists still subscribe to, is that selection can lead to aesthetic exaggeration, as well as enhancement and evolution of traits for adaptation to environmental conditions. This is based on artificial selection for beautiful animals, for example, extravagant plumage in pigeons and fowl. Animals can also be bred for fighting, like pit bulls. So Darwin’s idea was to explain how selection can lead to traits that seem to go against our idea of what would survive well.
Therefore what most biologists assume is that the beautiful don’t survive well at all. The handicap principle provides one way out of this. Net selection on phenotypes, even with a handicap trait, can still be stabilizing while selection on individual traits is directional.
@Joel J. Adamson,
I would bet that variance of mutational load between individuals is responsible for important differences in beauty. And although, no doubt, it isn’t responsible for the whole range of aesthetic countenance, but I would be curious to see how much it accounts for differences within a range of siblings.
Obviously for a single locus the frequency for a potentionally lethal allele is rather low within the population, but consider the circumstance where you have a trait where the developmental stability and expression is tightly controlled by a wide range of loci. Remove lethality of a homozygote and assume additivity (so that deleterious mutations are not masked by a “good copy”). Complex organisms are a literal flux of bubbling mutational froth against which selection barely keeps up.
Hence physical beauty is an assessment of genetic health, as only individuals with low a mutational load can devote the resources to the expression of a gaudy and aesthetically extravagant phenotype.
The extent to which attractive males bear genes that reduce other fitness components has remained unexplored, but anyway whichever negative correlation between attractiveness and viability does not falsify good genes (i.e. low mutational load), if mating with a high-quality male results on average in superior offspring performance (mating success of sons included). The heritable “good genes” benefit can be sustained even if sexually antagonistic genes cause female offspring sired by high-quality males to survive and reproduce less well.