This blog post explores how Richard Dawkins’ theory of sexual selection and Richard Zahavi’s handicap principle can coexist with the theory of natural selection.
In The Selfish Gene, Richard Dawkins argues that the protagonist of evolutionary theory is not the individual or the species, but the gene, and that living organisms are machines for preserving genes. Among the various ideas derived from this claim, we will focus on the ‘Handicap Principle’. In his ‘Theory of Sexual Selection’, Dawkins mentions the conflict between males and females in nature, proposing two strategies: females selecting males who make the household happy, and females selecting males with strong masculinity. Dawkins explains that these two strategies stem from the female’s goal of preserving her own genes and strong genes.
Dawkins states that those skeptical of selecting masculine males brought up Zahavi’s theory, the ‘Handicap Principle’. While he says the ‘Handicap Principle’ offers an explanation diametrically opposed to sexual selection theory, he also points out that arguments opposing this principle contain errors. This error relates to the claim that the ‘handicap principle’ and natural selection cannot coexist. Furthermore, Dawkins presents a different perspective on the ‘handicap principle’ in his 1976 publication The Selfish Gene compared to his current views. This essay proceeds based on the 1976 first edition. The handicap principle can effectively explain Dawkins’ theory of sexual selection, and his opposition stemmed from a misunderstanding of the principle. Therefore, we will examine Zahavi’s handicap principle, analyze Dawkins’ objections, and discuss sexual selection and natural selection. Finally, we will demonstrate that the two theories are mutually compatible.
First, let us examine the foundational theories of this topic: Dawkins’ theory of sexual selection and natural selection. In The Selfish Gene, Dawkins builds upon Darwin’s theory of natural selection, explaining that organisms evolve through the processes of replication, mutation, competition, and selection. As organisms reproduce, genes are passed to offspring, and individuals with mutations emerge. Those individuals adapted to the environment survive, a process seen as natural selection. In other words, individuals unable to adapt to the environment disappear. Ultimately, what Dawkins means by natural selection is that only genes possessing traits well-suited to the environment are passed on to offspring, thereby strengthening the group’s identity.
Next, to understand sexual selection theory, one must grasp the conflict between males and females based on the selfishness of genes. Let’s examine the selfishness of genes. The assumption that sexual reproduction and crossover coexist is difficult to explain. Sexual reproduction is a highly complex process for genes and can appear irrational. Sex is a cumbersome affair for passing on one’s genes. In contrast, asexual reproduction is more efficient than sexual reproduction. However, if we view each individual as a survival machine driven by an alliance of genes, sexual reproduction can also be understood as a trait regulated by genes. These genes compel other genes to submit to their selfish goals.
Now, let’s move on to the theory of sexual selection. Sex is asymmetrical. The most fundamental property demonstrating this asymmetry is the reproductive cells of males and females. Male sperm are numerous, highly motile, and small in size but nutritionally poor. Female eggs, conversely, are fewer in number, less motile, but larger and nutritionally rich. Dawkins posits that this disparity initiates a process where males exploit females.
At first glance, one might think males are unnecessary simply because sperm are numerous. However, the tendency for female numbers to remain constant can be explained by the selfish gene. If the sex ratio in a population tilts toward females, males—or rather, their sperm—are abundant, so no major problem arises. In this scenario, parents who have offspring with a small number of males gain a significant advantage. This is because they can produce many offspring. This process explains why females engage in sexual selection, choosing males with strong masculine traits. Dawkins argues that sexual selection does not contradict natural selection theory because good genes survive while bad genes are eliminated.
Now, let’s explore Zahavi’s handicap principle. In sexual selection, females desire males with strong genes. For example, males possessing genes that easily develop muscles will be physically large or have prominently developed muscles. Females select such males to choose those with strong genes. Zahavi argued that the handicap principle allows females to distinguish between males with this false appearance and truly strong males.
The handicap principle posits that handicaps exist to help females distinguish these males. Through the handicap, females judge that the male possesses strong genes capable of survival despite the handicap. For example, the male peacock’s colorful feathers make it easier for predators to locate him, yet males who survive despite this prove they possess strong genes. In other words, the handicap serves as evidence of strong genes.
Through this selection, the genes of females who choose males with handicaps are more likely to be passed on to offspring. Consequently, the population of males with handicaps increases, driving evolution toward individuals bearing such handicaps. Ultimately, females selecting males with handicaps choose those with superior traits, and these genes confer advantages to offspring. Thus, females can pass on good genes to their progeny.
Now, let’s examine Dawkins’ stance on the ‘handicap principle’. Thirty years after publishing The Selfish Gene, Dawkins revised his theory. Nevertheless, he remains skeptical of the handicap principle. Dawkins’ initial position was as follows. When females choose males, two strategies exist. One involves selecting males who pursue domestic harmony, while the other involves choosing males with strong masculinity. The strategy related to the handicap principle is selecting males with strong masculinity. Dawkins views the ultimate goal of males as continuing to survive and passing their genes on to offspring. However, the handicap principle posits that males display handicaps to be selected by females. Dawkins states that in this process, the handicap principle stands in opposition to the theory of sexual selection. He also argues that if a male can gain an advantage over other males without displaying a handicap, that is the optimal strategy.
Dawkins acknowledged that critics of Zahavi’s handicap principle might be incorrect. The strategic choice handicap principle suggests males can decide whether to develop a handicap directly. According to this, genes do not determine all traits but rather whether a trait is expressed. However, Dawkins argues that there is no need to worry about the risks or potential losses arising from the handicap principle, and that only natural selection can judge this. In other words, Dawkins did not acknowledge that the handicap principle could coexist with the theory of sexual selection.
Next, let’s examine why Dawkins rejected the handicap principle. Dawkins strongly rejects the idea that animal handicaps develop as Zahavi’s principle suggests. He argues that accepting this logic would imply that organisms with only one eye or ear would evolve instead of those with two. He specifically uses the example of the walrus to illustrate this.
Elephants do not acquire territory to impress females, but to defend their own territory by driving out other males. The owner of the territory gains a competitive advantage simply by having defended it. Consequently, a male walrus possessing a territory gains an advantage over other males without needing a handicap. Furthermore, females pass on genes to offspring by mating with these strong males, ensuring good genes are transmitted. Ultimately, if a male can gain an advantage through other means without displaying a handicap, he can develop his abilities.
Dawkins argued that the transmission of genes disadvantageous for survival contradicts natural selection theory. According to the above, the handicap principle can be understood as a partial principle of sexual selection theory. The reason females select males with handicaps lies not in the handicap itself, but in recognizing the male’s advantages through the handicap. In other words, the handicap serves as an indicator in sexual selection, helping females choose good males. Since Dawkins argued that sexual selection is included within natural selection, the handicap principle, being part of sexual selection, can coexist with natural selection. If an individual’s ultimate goal is to reduce its handicap for survival and pass on good genes, this also does not contradict natural selection. Whether a male becomes a good mate by retaining a handicap or discards it for survival depends on the individual’s fitness. High fitness increases the likelihood of survival even with a handicap.
Next, in critiques of Dawkins’ handicap theory, the point that “if a handicap is a true handicap, it could negatively affect offspring” is where Dawkins and Zahavi’s views diverge. This is because the good traits necessary to overcome the handicap are also likely to be inherited, making it possible for the handicap to be passed on to offspring. As explained in the elephant seal example, Dawkins argues that male elephant seals demonstrate superiority by occupying harems. Holding a harem can be considered a handicap that provides an advantage in competition. Ultimately, handicap theory also explains traits males possess to be selected by females. This can be seen as one method, within the framework of sexual selection as described by Dawkins, by which females choose masculine males.
Of course, viewed in isolation, the handicap theory might seem incompatible with sexual selection theory. The handicap theory argues that males attract females with inferior traits, and that a larger handicap allows for greater attraction. However, from the perspective of natural selection theory, the development of a handicap—a trait disadvantageous for survival—appears contradictory. However, when accepting the handicap theory, one must not focus solely on the fact that handicaps are traits that reduce survival probability. It is true that genes carrying handicaps lower survival probability.
For example, the large antlers of male deer are easily visible from a distance, making them prime targets for predators. However, handicap traits also have the advantage of highlighting strong genes in situations where females select males. If a male survives despite having a large handicap, it proves he has developed special traits advantageous for survival that allow him to overcome the handicap.
Consequently, from the female’s perspective, even if offspring inheriting the male’s trait slightly reduces their survival probability due to the handicap, if she judges that passing on the male’s genes to offspring is beneficial, the handicap can become a favorable factor in sexual selection. Consequently, handicaps do not contradict the theory of sexual selection. Since sexual selection is encompassed within the theory of natural selection, the handicap principle can also be harmonized with natural selection.
