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Chance, Variation and Shared Ancestry: Population Genetics After the Synthesis

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Abstract

Chance has been a focus of attention ever since the beginning of population genetics, but neutrality has not, as natural selection once appeared to be the only worthwhile issue. Neutral change became a major source of interest during the neutralist–selectionist debate, 1970–1980. It retained interest beyond this period for two reasons that contributed to its becoming foundational for evolutionary reasoning. On the one hand, neutral evolution was the first mathematical prediction to emerge from Mendelian inheritance: until then evolution by natural selection was considered the alternative to the fixity of species; now it appears to be the alternative to continuous change. Second, neutral change generated a set of clear predictions on standing variation. These could be used as a reference for detecting more elusive alternative mechanisms of evolution including natural selection. In the wake of the transition from Mendelism to genomics, the combination of coalescent theory, DNA sequence variation, and numerical analysis made it possible to integrate contingent aspects of the history of species into a new null model, thus opening a new dimension in the concept of population that the Modern Synthesis formerly considered as a mere gene pool.

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Notes

  1. Source: Web of knowledge.

  2. Tribute is paid to some of them in Nagylaki (1989), Kingman (2000), Slatkin and Veuille (2002), and Grodwohl (2017).

  3. Sampling is at the root of Fisher’s conception of inference methods in statistics; he opposed the belief of biometricians that population parameters should be estimated from large numbers. He also opposed the tendency to favor the Bayesian approach, which he dismissed as “inverse probability.” Following William Gosset’s "student’s test," he developed inference methods from samples of small size, for which the introduction of degrees of freedom was essential (see Fisher 1956).

  4. Throughout this study, equations are used only to illustrate relationships between basic concepts, and so are kept simple.

  5. Note that recombination is a biological mechanism that decreases the effect of sampling by freeing genes from linkage to selected loci.

  6. Named after two animal geneticists who were among the first to suppose that a small group would tend to genetic homogeneity. As they wrote: "to explain how all the individuals on one island have come to be pure for one set of characters, we need not ascribe any selection value to those characters" (Hagedoorn and Hagedoorn-Vorstheuvel La Brand 1921, p. 123).

  7. According to Wright, the meaning of “drift,” initially a simple expression, evolved gradually into “random drift,” a concept, from 1929 to 1956 (see Wright 1977, p. 444); Fisher (1930) mentions the “so-called genetic drift” in the 1958 edition, p. 10.

  8. In a Markov process, the state of a random variable depends on the immediately preceding step, but memory is lost of the more ancient steps.

  9. For example, Dobzhansky (1954, p. 26) referred to the “genetic alphabet” as follows: “Evolution may be viewed as a result of these letters combining into new words. The genes which may be compared with words in the genetic message, etc.”.

  10. "Molecular" refers to expressions used at that time, including “molecular approach to the study of genic heterozygosity” (Hubby and Lewontin 1966), even though proteins were the only molecular level considered in these studies. The adjective "genomic," as used here, has a broad meaning; it refers to "genome," or the organization of genetic material, not just to "genomics," the interpretation of high-throughput sequencing; on genomics, see the special issue on Genomics and the Human Genome Project, Journal of the History of Biology 51 (4), 2018.

  11. Since bacteria do not follow Mendelian mechanisms of sexuality, their study was already based on properties of biochemical metabolism, thus the molecular period led to unification in genetics, whereas sex (in its form generating Mendel’s rules) from then on appeared merely a recent outcome in the history of life.

  12. According to Michel Gillois (1996), it was Oscar Kempthorne (1957) who popularized Malécot’s "identity" concept as "identity by descent" ("IBD"), as opposed to "identity by state" ("IBS") following Cotterman (1940). This often leads to the misconception that IBD and IBS are alternative states for genes, which they are not.

  13. The difference between Malécot’s probabilistic approach and Wright’s statistics in population structuring is analyzed in Ishida (2009); I do not develop here Wright’s theory of path coefficients, which will require another occasion to compare them.

  14. In this sentence, Mayr attempted to give a definition of “population” that could be universally viewed as being consistent with the Modern Synthesis, even though he expressed on many occasions his own opinion that “there is a harmony among the genes which together make up the local gene pool” (Mayr 1959, p. 8), which may be regarded as an organicist conception of the population. This view was shared by Dobzhansky: “The gene pool is not an accidental conglomeration of individual genotypes. It is rather an organized system, a system so contrived as to yield the highest mean level of adaptedness in the individuals” (Dobzhansky 1954, p. 96).

  15. By definition, the number of matings effected by males is strictly equal to the number of matings effected by females, but the mating population in each sex may be different.

  16. See: John van Wyhe, ed. 2002–. The Complete Work of Charles Darwin Online: http://darwin-online.org.uk/graphics/Origin_Illustrations.html

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Acknowledgments

This study is dedicated to Jean Gayon (1949–2018) and was inspired by a series of seminars held in the Muséum National d’Histoire Naturelle, Paris, in June 2016 by Jean and myself on the evolution of evolutionary theory in the last half-century. I am greatly indebted to Richard Burian, Michael Dietrich, Jean-Baptiste Grodwohl, and Philippe Huneman for comments that greatly improved the manuscript. I thank Guillaume Achaz, Claudine Cohen, David Depew, Maureen O’Malley, Anya Plutinsky, and Amir Yassin for kindly commenting on former versions and exchanging ideas.

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Authors and Affiliations

  1. Institut Systématique Évolution Biodiversité (ISYEB, UMR 7205, CNRS, EPHE, MNHN, UPMC), Ecole Pratique des Hautes Etudes, Université Paris Sciences Lettres, Paris, France

    Michel Veuille

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  1. Michel Veuille
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Correspondence to Michel Veuille.

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Veuille, M. Chance, Variation and Shared Ancestry: Population Genetics After the Synthesis. J Hist Biol 52, 537–567 (2019). https://doi.org/10.1007/s10739-019-09584-3

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