Neutral Theory

by

Jianzhi Zhang

• LAST REVIEWED: 16 March 2022
• LAST MODIFIED: 28 June 2016
• DOI: 10.1093/obo/9780199941728-0081

Introduction

The neutral theory, formally known as the neutral theory of molecular evolution, was independently proposed by M. Kimura in 1968 (see Kimura 1983, cited under General Overviews, the Neutral Hypothesis of Phenotypic Evolution, and Outstanding Questions; Kimura 1994, cited under General Overviews; and Kimura 1968, cited under Origin of the Theory) and J. L. King and T. H. Jukes in 1969 (see King and Jukes 1969, cited under Origin of the Theory). The chief tenet of the theory is that most genetic differences between species and polymorphisms within species are selectively neutral and result from mutation and genetic drift. This view sharply contrasts that of neo-Darwinists, who maintain that most of these variations are adaptive. While the neutral theory has been controversial since its debut, the neutralist-selectionist debate has been largely healthy in that it greatly stimulated the development of rigorous neutrality tests, and it is now customary to invoke adaptive explanations only when a null hypothesis of neutrality is rejected. The neutral theory has been revised and broadened in a number of ways since the 1990s, including the emphasis of nearly neutral mutations in the nearly neutral theory, expansion to evolutionary explanations of genomic architectures, and application to phenotypic evolution. While these studies are not without contention, the idea that genetic drift, rather than adaptation, could explain origins of nonrandom patterns in biology has had profound impacts on many biologists’ view of evolution and the living world. The neutral theory remains the sole paradigm-changing conceptual revolution in evolutionary biology since the maturation of the neo-Darwinism in the 1950s.

General Overviews

There are a few books on the neutral theory, and Kimura 1983 remains the most comprehensive and authoritative book on the topic. Kimura 1994 is an edited volume of Kimura’s original papers on neutral theory and his underlying population genetic work. Crow and Kimura 1970 is a classic textbook of population genetic theory and deals with many fundamental concepts; it is highly useful for understanding the population genetic basis of the neutral theory. Ohta 2009 is a Japanese book on nearly neutral theory, which asserts that most intraspecific and interspecific genetic variations are not strictly neutral but are nearly neutral. Lynch 2007 argues that fixations of slightly deleterious mutations by drift led to the origins of various complex genomic architectures. Nei 2013 argues for the role of mutation and drift in evolution in general. Textbooks of molecular evolution that contain lucid discussions about the neutral theory and related topics include Nei 1987 and Li 1997.

• Crow, J. F., and M. Kimura. 1970. An introduction to population genetics theory. Caldwell, NJ: Blackburn.

  A classic textbook of theoretical population genetics, it provides many theoretical results pertaining to the neutral theory.

• Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge, UK: Cambridge Univ. Press.

  DOI: 10.1017/CBO9780511623486

  In this single most important book of evolutionary biology since the 1960s, the neutral theory is lucidly, comprehensively, and forcefully argued for by its chief advocate.

• Kimura, M. 1994. Population genetics, molecular evolution, and the neutral theory: Selected papers. Chicago: Univ. of Chicago Press.

  An edited volume of Kimura’s original papers, many key to the development of the neutral theory.

• Li, W.-H. 1997. Molecular evolution. Sunderland, MA: Sinauer.

  A lucid and comprehensive textbook on molecular evolution, it discusses many topics highly relevant to neutral theory, such as nucleotide and amino-acid substitution rates and the molecular clock.

• Lynch, M. 2007. The origins of genome architecture. Sunderland, MA: Sinauer.

  The role of nearly neutral mutations in the origins of genomic complexity is forcefully argued for in this monograph.

• Nei, M. 1987. Molecular evolutionary genetics. New York: Columbia Univ. Press.

  A pioneering textbook of molecular evolutionary genetics by a longtime supporter of the neutral theory.

• Nei, M. 2013. Mutation-driven evolution. Oxford: Oxford Univ. Press.

  The author proposes a central role of mutation (and drift) rather than selection in evolution in general.

• Ohta, T. 2009. Nearly neutral theory of molecular evolution: Evolutionary models of selection and chance. Tokyo: Kodansha.

  A text on the nearly neutral theory, written by the proposer of the theory. In Japanese.