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First published online April 20, 2007
Journal of Experimental Biology 210, 1653-1660 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02725

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Review Article

Evolvability of physiological and biochemical traits: evolutionary mechanisms including and beyond single-nucleotide mutation

Martin E. Feder

Department of Organismal Biology and Anatomy and The Committees on Evolutionary Biology, Genetics, and Molecular Medicine, The University of Chicago, 1027 E. 57th Street, Chicago, IL 60637, USA

e-mail: m-feder{at}uchicago.edu

Accepted 17 January 2007

A longstanding challenge for biologists has been to explain not just how organisms are adapted to diverse environments, but how these adaptations arise. Although natural selection is clearly sufficient to act on heritable variation, is this heritable variation sufficient to yield complex adaptations and how does this variation itself arise? Much prior focus has been on mutation of single nucleotides in genes. This process is common and can have dramatic phenotypes, but could be limited in its ability to culminate in complex adaptations for two kinds of reasons: (i) because natural selection is powerful, it can purge genetic variation, and (ii) evolutionary transition from the absence to the presence of a complex adaptation seemingly requires multiple mutations at the right place and time and in the right sequence, with each intermediate stage having increased overall fitness; this seems highly improbable. Because the networks that organisms comprise are hierarchical and redundant and have modular structure, however, single-nucleotide mutations can have large and tolerable impacts. Diverse mechanisms, collectively evolutionary capacitors, can shield genetic variation from the purgative of selection. These features can enable evolution to proceed via single-nucleotide mutation. Importantly, single-nucleotide mutation usually only modifies existing genes rather than creating new ones, and numerous other mechanisms eclipse single-nucleotide mutation in creating genetic variation. These include gene duplication (both segmental and whole-genome), lateral gene transfer, hybridization, mobile genetic elements and symbiosis. Other processes can scramble and reassemble nucleotide sequence. The mechanisms beyond single-gene mutation offer considerable promise in detailing the evolution of complex physiological and biochemical traits, and have already done so for several morphological traits.

Key words: evolution, mutation, adaptation, natural selection, evolvability, gene duplication, transposable element

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