Natural selection. III. Selection versus transmission and the levels of selection. Journal of Evolutionary Biology

Natural selection increases inherited information about environmental challenge. Against selection, imperfect transmission reduces inherited information. Many problems in biology come down to understanding the relative balance between selection and imperfect transmission. A clear understanding of selection and transmission requires greater precision with regard to abstract notions such as inherited information. However, before heading off in pursuit of abstract theory, it pays to have some simple examples in mind. Those simple examples define the challenges for deeper theory. In this paper, I work through several examples that turn on the relative strength of selection and imperfect transmission: Haldane (1927) and Lande’s (1975) balance between selection and mutation, Eigen’s (1992) error threshold and quasispecies, Van Valen’s (1975) multilevel analysis of clade selection, Price’s (1972) multilevel analysis of group selection, Szathmáry & Demeter’s (1987) stochastic corrector model of early cellular evolution, Levin & Bull’s (1994) short-sighted model of parasite evolution, Frank’s (2010) timescale model of microbial metabolism and Maynard Smith & Szathmáry’s (1995) major transitions in evolution. Others have pointed out similarities between some of these examples (Maynard Smith & Szathmáry, 1995; Michod & Herron, 2006; Okasha, 2006). However, the broad unity with regard to selection and transmission is sometimes lost. In addition, the key role of timescale, although often noted, has not always been linked to selection and transmission in a simple and general way. Williams’ (1966) quote emphasizes timescale: the opposition between selection bias and rate of endogenous change. An entity can be shaped by natural selection only to the extent that the informational gain by natural selection is not overwhelmed by the relative rate of informational decay by imperfect transmission. The balance between selection and decay often turns on the relative timescales over which those forces operate. Correspondence: Steven A. Frank, Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697–2525, USA. Tel.: +1 949 824 2244; fax: +1 949 824 2181; e-mail: [email protected] *Part of the Topics in Natural Selection series. See Box 1.