Sexual selection and natural selection



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Sexual selection and natural selection

  • Jean Gayon Institute of History and Philosophy of science & Techniques
  • Un. Paris 1-Panthéon Sorbonne

1. Introduction: the two sides of Darwin’s theory of selection in nature

  • Natural selection/sexual selection: “two natural means of selection”
    • On the Origin of Species by Means of Natural Selection (1859): 491 pages
    • The Descent of Man, and Selection in Relation to Sex (1871): 571 pages (over 830) devoted to sexual selection
  • Different fates of the two theories
  • Two questions:
    • Why was sexual selection so important to Darwin?
    • Why was it so much deemphasized by Darwin followers?
  • Outline
      • Sexual selection in Darwin’s thought
      • Wallace’s criticism of sexual selection
      • Sexual selection as an indicator of different conceptions of natural selection

2. The rise of sexual selection in Darwin’s thought

  • “Old and Useless Notes” (1838-1840) Darwin sensitive to two problems:
    • How does a female recognize a beautiful male? “How does Hen determine most beautiful cock, which best singer?”
    • Similarity between:
      • Choice of a sexual partner by an animal
      • Artificial selection

2. The rise of sexual selection in Darwin’s thought

  • Essays of 1842 and 1844
    • The term “sexual selection” does not yet appear
    • Distinction between two kinds of “struggle of the males for the females”: “battle” vs “courtship”
    • In 1844, this process is presented as another “natural means of selection” In this text, this other process is presented as another way for producing adaptations

2. The rise of sexual selection in Darwin’s thought

  • « Besides this natural means of selection, by which those individuals are preserved, whether in their egg or seed or in their mature state, which are best adapted to the place they fill in nature, there is a second agency at work in most bisexual animals tending to produce the same effect, namely the struggle of the males for the females » (Darwin, 1844 Essay)

2. The rise of sexual selection in Darwin’s thought

  • On the Origin of Species (1859)
    • Sexual selection disconnected from struggle for existence: « ...what I call Sexual Selection. This depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring. Sexual selection is, therefore, less rigorous than natural selection.
    • 1st mode: direct rivalry between males: « ...Generally, the most vigorous males, those which are best fitted for their places in nature, will leave most progeny. But in many cases, victory will depend not on general vigour, but on having special weapons, confined to the male sex. » (OS, p. 88)

2. The rise of sexual selection in Darwin’s thought

  • On the Origin of Species (1859)
    • 2nd mode: female choice « I can see no reason to doubt that female choice, by selecting, during thousands of generations, the most melodious or beautiful males, according to their standard of beauty, might produce a marked effect. » (OS, p. 88)
    • This sentence was the main reason of the controversy between Wallace and Darwin over sexual selection, because of its anthropomorphic connotations:
      • cognitive abilities and aesthetic sense in animals

2. The rise of sexual selection in Darwin’s thought

  • Descent of Man (1871)
    • Huge documentation on secondary sexual characters
    • Darwin’s method: consilience of inductions (explaining a vas range of previously uncorrelated phenomena). Predictions:
      • Struggle more severe if sex ration ≠ 1
      • Struggle more severe in polygamous species
      • Struggle more severe in animals with more cognitive abilities.
      • ...

2. The rise of sexual selection in Darwin’s thought

  • Descent of Man (1871) Question: why did Darwin put in the same book his reflection over the origin of Man and that on sexual selection?
  • Darwin’s answer to the question of the origin of man is subtle:
    • Origin of generic physical traits: individual natural selection
    • Origin of mental characters: individual natural selection (but also benefits to the group)
    • Origin of moral characters: “tribal” (or group) natural selection
    • Origin of human races (physical traits): sexual selection
    • Origin of mental and moral traits among races: natural selection (tribes)

2. The rise of sexual selection in Darwin’s thought

  • Descent of Man (1871)
  • Content of the sexual selection hypothesis :
    • Definition: “[it] depends on the advantage which certain individuals have over either individuals of the same sex and species, in exclusive relation to reproduction”
    • Two modes:
      • rivalry between males founded on vigor and strength;
      • mate choice (mainly female choice, but not exclusively)
    • These two modes are not sharply divided
    • Neither is the distinction natural/sexual selection absolute

3. The Darwin-Wallace controversy

3. The Darwin-Wallace controversy

  • Overview of the disagreements between Wallace and Darwin
    • Theory of selection
      • Environmental vs competitive concept of natural selection
      • Group and species selection
      • Sexual selection
    • Role of natural selection in the explanation of particular phenomena
      • Origin of hybrid sterility
      • Origin of sexual dimorphism
      • Origin of Man and of human races
    • Place of the principle of natural selection in evolutionary theory
      • Wallace more radical than Darin on natural selection as an all-sufficient principle for evolutionary theory

3. The Darwin-Wallace controversy

  • Overview of the disagreements between Wallace and Darwin
    • Theory of selection
      • Environmental vs competitive concept of natural selection
      • Group and species selection
      • Sexual selection
    • Role of natural selection in the explanation of particular phenomena
      • Origin of hybrid sterility
      • Origin of sexual dimorphism
      • Origin of Man and of human races
    • Place of the principle of natural selection in evolutionary theory
      • Wallace more radical than Darin on natural selection as an all-sufficient principle for evolutionary theory

3. The Darwin-Wallace controversy

  • Overview of the disagreements between Wallace and Darwin
    • Theory of selection
      • Environmental vs competitive concept of natural selection
      • Group and species selection
      • Sexual selection
    • Role of natural selection in the explanation of particular phenomena
      • Origin of hybrid sterility
      • Origin of sexual dimorphism
      • Origin of Man and of human races
    • Place of the principle of natural selection in evolutionary theory
      • Wallace more radical than Darin on natural selection as an all-sufficient principle for evolutionary theory

3. The Darwin-Wallace controversy

  • Overview of the disagreements between Wallace and Darwin
    • Theory of selection
      • Environmental vs competitive concept of natural selection
      • Group and species selection
      • Sexual selection
    • Role of natural selection in the explanation of particular phenomena
      • Origin of hybrid sterility
      • Origin of sexual dimorphism
      • Origin of Man and of human races
    • Place of the principle of natural selection in evolutionary theory
      • Wallace more radical than Darin on natural selection as an all-sufficient principle for evolutionary theory

3. The Darwin-Wallace controversy

  • Wallace’s attacked sexual selection on two fronts
    • Direct rivalry between males
      • Does exist, but superfluous in most cases. Natural selection can account for the observed phenomena e.g. male weapons are useful for defending the group (or the species) against predators)
    • Female (or mate) choice
      • Does not exist. Two lines of arguments:
        • Superfluous e.g. The dull appearance of many female birds is best explained by the necessity of protecting the nest against predators, while the conspicuous appearance of males allows them to attract predators and divert them from the nest
        • “Choice”, “beauty”, “aesthetic taste” are anthropomorphic notions. Such notions have no room in biological theory.

3. The Darwin-Wallace controversy

  • Wallace’s final judgement in his Darwinism (1889):
  • “My whole work tends forcibly to illustrate the overwhelming importance of natural selection over all agencies... even in rejecting that phase of sexual selection depending on female choice. I insist on the greater efficacy of natural selection. This is pre-emintently the Darwinian doctrine, and I therefore claim for my book the position of being the advocate of pure Darwinism”

4. Conclusion:striking the balance

  • Retrospectively, Wallace and Darwin were both right and wrong
    • Wallace was right to emphasize the adaptive importance of a number of aspects of sexual dimorphism Zahavi’s theory of “honest signaling” (1975) illustrates this point
    • But Wallace was unable to account for the most spectacular aspects of sexual dimorphism: extravagant colors, ornaments, and courtships.
    • Darwin was right to emphasize the proper evolutionary dynamics based on mate choice.
    • But his explanation based on purely psychological notions (choice and aesthetic sense) lacked evolutionary generality
    • R.A. Fisher (1930) was the first author to provide a convincing argument

4. Conclusion:striking the balance

  • Fisher’s argument (GTNS, 1930) In a population where there is a “majority preference” for anything whatsoever, the best reproductive strategy for a female is to adopt this preference, because “the next generation of daughters will inherit the mother’s preference whilst her sons will inherit their father’s attractive feature”

4. Conclusion:striking the balance

  • Sexual selection as an indicator of Wallace’s and Darwin’s concept of natural selection
    • Wallace: environmentalist conception of natural selection
    • Darwin: competitive conception of natural selection Sexual selection as a key test for Darwin’s conception of natural selection, based upon intraspecific competition


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