Levels of Selection in Evolution

By B. Charlesworth. Heredity, 2000

233 citations recorded by the source corpus.

The question of the interplay between the eects of selection at dierent levels of biological organization emerged early in the development of population genetics. Haldane, in Chapter 5 of The Causes of Evolution, gave a particularly lucid account. He pointed out that competitive selection between individuals within a population, notably sexual selection, may lead to the evolution of traits that are deleterious with respect to the longterm survival of the species. He emphasized that selection between dierent gametic genotypes, even among those produced by the same individual, can lead to the spread of traits that are deleterious to the individual, especially in higher plants where genes are expressed in the pollen. He also discussed the evolution of altruistic traits by kin selection and group selection. In addition to con ̄icts between dierent levels of selection, there is also the possibility of con ̄ict between entities at the same level of organization, but which are subject to dierent rules of inheritance. This was probably ®rst noticed by D. H. Lewis in 1941, when considering the spread of nuclear and cytoplasmic genes that control male sterility in plants. Levels of Selection in Evolution is the ®rst book to provide an overview of the very diverse recent literature on these topics, which ultimately traces back to these pioneering contributions (neither Haldane's nor Lewis' work is cited, however!). It contains papers that deal with the evolution of replicators (Szmathmary), individuals (Michod), and animal (Kitchen and Packer) and human societies (Maynard Smith). Other papers treat con ̄icts and communities of interest between genes within the same organism (Pomiankowski), between the sexes (Lessells), parents and ospring (Godfray), members of social groups (Keller and Reeve), and species in ecological communities (Herre). The properties and consequences of selection at dierent levels are discussed in general papers by Leigh, Nunney, and Reeve and Keller. The book contains a large quantity of fascinating biological information and descriptions of clever theoretical models, and will undoubtedly be a very useful resource for researchers in evolutionary biology. One question that it raises, however, is whether there is a useful general theory of con ̄ict that can be applied painlessly to solve particular problems. My impression is that there is not; I can see very little in common between, for example, the application of ESS 1 theory to parent±ospring con ̄ict, and the use of population genetic dynamic modelling to study transposable elements or segregation distorters. The generalizations that are provided in the overview papers are, inevitably, bland and not very informative. I also have the impression that dierent topics are at very dierent levels of scienti®c development, in the sense of confronting theories with tests. Topics such as sex ratio distortion and worker con ̄ict in insect societies seem to be in a healthy state, where details of biology can be successfully interpreted by plausible models. In contrast, I am not convinced that the discussions of the evolution of replicators and individuals, at one extreme, or human language at the other, are more than ingenious speculation, with little hope at present for hypothesis testing. It is interesting that dierent authors contradict each other on some of these topics; Michod, for example, accepts the role of hypercycles in prebiotic evolution, whereas Szmathmary is critical. Leigh believes that anisogamy arose to promote uniparental transmission of cytoplasmic organelles, whereas Lessells emphasizes the importance of the con ̄ict between gamete number and gamete size. Of the more theoretical papers, Godfray's stands out as an example of caution in relating the ideas to the data. I would have liked to see this caution applied more widely; the development of hypotheses is essential for progress, but one should not confuse them with reality.

Subfields: Sociology and Political Science

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Citations in the corpus

Reciprocity and conditional cooperation between great tit parents (2014, unknown): “Parents rearing young together, for instance, face an evolutionary conflict of interest, because each benefits from joint investment in the offspring, but pays a cost of providing that care in terms of reduced survival or fecundity (Trivers 1972; Lessells 1999).”
A Symbiotic View of Life: We Have Never Been Individuals (2012, background): “This problem of cheaters, it has been argued, has rendered many models of group selection mathematically untenable (see Keller 1999; Leigh 2010; Eldakar and Wilson 2011).”
Dangerous liaisons: the ecology of private interest and common good (2001, unknown): “That ecological interactions are often complex mixtures of conflicting and overlapping interests is increasingly being recognized by evolutionary biologists (see reviews by Bronstein 1994a, b, Leigh and Rowell 1995, Frank 1997, Herre et al. 1999, Keller 1999).”
Rethinking the Theoretical Foundation of Sociobiology (2007, background): “The only way to maintain these two positions is by claiming that modern multilevel selection theory bears no relationship to its own past (e.g., Keller 1999; West et al. 2006, 2007).”