Video Lecture

Sexual Selection

Darwin suggested that some traits were passed from one generation to the next, not because they conferred the individual higher chances to survive, but because they enhanced their chances of mating. Sexual selection is, thus, not a particularity of natural selection, for it derives from differences in mating success, whereas natural selection derives from variance in all other fitness components. Darwin insisted that sexual selection differed from natural selection. He writes that sexual selection “[…] depends not on the struggle for existence, but on the struggle between males for possession of females.” (Darwin, 1871). Even though Darwin mentions males in this sentence, he was well aware of the female reproductive competition. Darwin observed that although males can be choosy and females competitive, females are typically the pickiest and males the most competitive. As a result, as a first approach, mate choice is female, and competition is male, although not exclusively.

Darwin proposed that differences between males and females in “habits” and features other than their primary sexual traits were likely the result of natural selection. Furthermore, that natural selection was responsible whenever a characteristic appeared for “the general purposes of life.” However, a trait was subject to sexual selection if it conferred an advantage over a rival in finding a mate. Darwin also predicted that many traits would likely be subject to both types of selection and that it would frequently be difficult to tell them apart. Thus, selection includes both sexual and natural selection and sets these mechanisms apart from neutral processes that lead to organic evolution (e.g., genetic drift).

Sexual selection occurs in two variants. Members of one biological sex choose partners from the other sex to mate with (intersexual selection) and compete with one another for access to partners from the other sex through sexual selection (intrasexual selection). These two types of selection result in some individuals within a population having a higher rate of reproductive success than others because, for instance, they are more attractive or choose more attractive mates to bear their offspring. 

Frequent mating and having exclusive access to one or more reproductive females are advantageous to successful males. By choosing and mating with the best males, females can maximize the return on the energy they invest in reproduction. Therefore, choosing the right partner is crucial for how one’s genes will fare in the next generation’s gene pool.

Early in the 20th century, Ronald Fisher provided Darwin’s theory of sexual selection with a mathematical foundation. Males may go to great lengths to prove that they are suitable for female selection, which results in sexual dimorphism and secondary sexual traits like the elaborate plumage of birds-of-paradise or the antlers of deer. A positive feedback mechanism, the Fisherian runaway effect, brings this about. This runaway effect comes equally from the desire for a feature to be present in one sex as from the presence of the trait in the other sex. Runaway selection occurs when a female preference and a male trait evolve together (Fisher, 1930). Fisher’s principle explains why the sex ratio is most frequently 1:1, even if the “sexy son” hypothesis suggests that females favor male offspring. There is a widespread sexual selection among fungi, plants, and animals.

Fisher envisioned an initially natural selection-favored masculine feature. Any female aware of that trait would be fitter since her offspring would inherit both the trait and the propensity to pay attention to it. As a result, the trait would acquire a natural selection advantage and an additional benefit due to female preference, which would be proportional to the strength of preference, and both the trait and preference would spread across the population. That would result in the evolution of the male trait and the female preference because, as Fisher put it, “Whenever appreciable differences exist in a species, which are in fact correlated with selective advantage, there will be a tendency to select those individuals of the opposite sex who most clearly discriminate the difference to be observed.” (Fisher, 1930).

Because it typically pushes trait values above their natural selection optimum, sexual selection is frequently stronger than natural selection. The quantitative paradox of sexual selection refers to the fact that it occurs despite primarily affecting just half of the population, typically males. Most females mate and produce offspring, although, in many species, most males never have a chance to mate.

The solution to this apparent paradox is that variance in male reproductive success is often considerable, explaining why sexual selection can be so strong. Male traits are frequently under intense selective pressure, with many male traits being sexually selected. Because of this, male mammals are often larger and more evident in their sexual displays than females.

While the reason why males compete is apparent—they require females to maintain fitness—it is unclear what benefits females draw. Female choice benefits can be direct, e.g., enhanced female fecundity or lifespan, and indirect, e.g., improvement in offspring quality. This quality may include sexual quality, more attractive sons (the Fisher effect), or good genes in general.

Some questions remain unanswered, such as whether females choose mates rationally or make decisions that are not in their best interests. We do not yet have definitive answers to these questions. Most importantly, it is unclear whether sexual selection is adaptive. While Darwin believed sexual selection might improve the breed or species, he also used it to explain traits that were not adaptive.

Watch Richard Dawkins on population control.

Secondary Sexual Traits

Secondary sexual traits and ornaments are selected for their ability to facilitate mating (e.g., horns, antlers, over-dimensioned fangs, and large breasts). 

These traits are especially noticeable in the sexually dimorphic phenotypic traits that separate a species’ sexes. They do not function as a direct component of the reproductive system, unlike the sex organs (primary sex traits). Secondary sex traits emerge from sexual selection for qualities that demonstrate fitness, providing an organism an advantage over rivals in competing encounters and courtship. Some examples of secondary sex traits are the manes of male lions, the bright colors on the faces and rump of male mandrills, and the horns of many species.

The handicap principle explains how something like a peacock’s tail, a worthless but extremely difficult-to-fake obstacle, demonstrates fitness (Zahavi, 1975). According to the sexy son theory, females will want to have sons who have the traits they find sexually alluring in order to increase the number of grand-offspring they have (Weatherhead & Robertson, 1979). An alternate theory is that some genes that help males acquire impressive ornaments or the capacity to fight may be associated with fitness indicators like disease resistance, a more effective metabolism, or higher-quality sperm.

The majority, if not all, of secondary sexual traits, are probably sexual and natural selection targets. In most circumstances, natural and sexual selection will combine to drive evolution and changes in secondary sexual traits. Secondary sexual characteristics may have evolved due to altered interactions between these selective pressures. Suppose natural selection against excessive secondary sexual features waned when a group of animals invaded a new and favorable environment. In that case, one would expect to witness fast evolutionary change wholly driven by sexual selection. 

Secondary sexual traits can evolve due to natural selection alone (Garant et al., 2004), due to sexual selection alone (Martin & Hosken, 2003), or (perhaps most commonly) due to a change in the balance between natural and sexual selection (Kinnison et al., 2003).

Fruit fly females, Drosophila, only accept being mated by males able to perform an elaborate courtship dance to perfection. Studies show that good male dancers have better sperm quality than bad ones. That shows that primary sex cells can bear secondary sexual strains. 

References

Arnqvist, G. & Rowe, L. (2005). Sexual Conflict. Princeton University Press, Princeton. ISBN: 9780691122182. 

Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. John Murray, London. DOI: https://doi.org/10.5962/bhl.title.110063.

Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford, UK: Clarendon Press. ISBN: 9780198504405.

Garant, D., Sheldon, B.C. & Gustafsson, L. (2004) Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58, 634– 644.

Hoquet, T. (2015). Current Perspective on Sexual Selection—What’s left after Darwin? Springer Dordrecht. ISBN: 978-94-017-7990-6.

Hosken, D. J. & House, C. M. (2011). Sexual selection. Current Biology, Volume 21, Issue 2, 2011, Pages R62-R65, ISSN 0960-9822. https://doi.org/10.1016/j.cub.2010.11.053.

Kinnison, M.T., Unwin, M.J. & Quinn, T.P. (2003) Migratory costs and contemporary evolution of reproductive allocation in male chinook salmon. Journal of Evolutionary Biology 16, 1257– 1269. https://doi.org/10.1046/j.1420-9101.2003.00631.x

Lande, R. & Arnold, S.J. (1983) The measurement of selection on correlated characters. Evolution 37, 1210– 1226. https://doi.org/10.2307/2408842.

Martin, O.Y. & Hosken, D.J. (2003) The evolution of reproductive barriers through sexual conflict. Nature 423, 979– 981. DOI: 10.1038/nature01752.

Pattarini, J. M., Starmer, W. T., Bjork, A., Pitnick, S. (2006). Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution. 2006 Oct;60(10):2064-80. PMID: 17133863.

Pavlou, H. J. & Goodwin, S. F. (2013). Courtship behavior in Drosophila melanogaster: towards a ‘courtship connectome’. Curr Opin Neurobiol. 2013 Feb;23(1):76-83. doi: 10.1016/j.conb.2012.09.002. Epub 2012 Sep 28. PMID: 23021897; PMCID: PMC3563961.

Svensson, E. I. & Gosden, T. (2007), Contemporary evolution of secondary sexual traits in the wild. Functional Ecology, 21: 422-433. https://doi.org/10.1111/j.1365-2435.2007.01265.x

Weatherhead, P. J., Robertson. R. J. (1979). Offspring quality and the polygyny threshold: ‘the sexy son hypothesis.’ The American Naturalist. 113 (2): 201–208. doi:10.1086/283379. JSTOR 2460199. S2CID 85283084.

Zahavi, A. (1975). Mate selection—A selection for a handicap. Journal of Theoretical Biology. Elsevier BV. 53 (1): 205–214. doi:10.1016/0022-5193(75)90111-3. ISSN 0022-5193. PMID 1195756.