Evolution, the Extended Synthesis

3 - High-Dimensional Fitness Landscapes and Speciation

3 High-Dimensional Fitness Landscapes and Speciation Sergey Gavrilets The Modern Evolutionary Synthesis of the 1930s and 1940s remains the paradigm of evolutionary biology (Futuyma 1998; Gould 2002; Pigliucci 2007; Ridley 1993). The progress in understanding the process of evolution made during that period had been a direct result of the development of theoretical population genetics by Fisher, Wright, and Haldane, who built a series of mathematical models, approaches, and techniques showing how natural selection, mutation, drift, migration, and other evolutionary factors are expected to shape the genetic and phenotypic characteristics of biological populations.These theoretical advances provided “a great impetus to experimental work on the genetics of populations ” (Sheppard 1954) and a “guiding light for rigorous quantitative experimentation and observation” (Dobzhansky 1955), and had many other far-reaching implications. According to Provine (1978), the work of Fisher,Wright, and Haldane had significant influence on evolutionary thinking in at least four ways. First, their models showed that the processes of selection, mutation, drift, and migration were largely sufficient to account for microevolution. Second,they showed that some directions explored by biologists were not fruitful.Third, the models complemented and lent greater significance to particular results of field and laboratory research.Fourth,they stimulated and provided framework for later empirical research. Since the time of the Modern Synthesis, evolutionary biology has arguably remained one of the most mathematized branches of the life sciences, in which mathematical models and methods continuously guide empirical research, provide tools for testing hypotheses, explain complex interactions between multiple evolutionary factors, train biological intuition, identify crucial parameters and factors, evaluate relevant temporal and spatial scales, and point to the gaps in biological knowledge, as well as provide simple and intuitive tools and metaphors for thinking about complex phenomena. 46 Sergey Gavrilets In this chapter, I discuss two particular areas of theoretical evolutionary biology that have experienced significant progress since the late 1980s: a theory of fitness landscapes and a theory of speciation. I also outline two particular directions for theoretical studies on the origins of biodiversity which are especially important, in my opinion, for unification of different branches of the life sciences. One is the development of a theory of large-scale evolutionary diversification and adaptive radiation. The other is a quantitative theory of the origins of our own species. Classical Fitness Landscapes The theoretical notion of fitness landscapes (also known as “adaptive landscapes,” “adaptive topographies,” and “surfaces of selective value”), which emerged at the onset of the Modern Synthesis, has become a standard tool both for formal mathematical modeling and for the intuitive metaphorical visualizing of biological evolution, adaptation, and speciation. This notion was first introduced by Sewall Wright in a classic paper delivered at the 1932 International Congress of Genetics. Wright wanted to illustrate his ideas and mathematical results on the interaction of selection, random drift, mutation, and migration during adaptation in a nontechnical way accessible to biologists lacking quantitative skills (Wright 1932, 1988). Wright’s metaphor of fitness landscapes is widely viewed as one of his most important contributions to evolutionary biology (Coyne et al. 1997; Pigliucci and Kaplan 2006; Provine 1986). Over the ensuing 70 years, the notion of fitness landscapes has been substantially expanded and has found numerous applications well outside of evolutionary biology (e.g., in computer science, engineering, economics, and biochemistry). A key idea of evolutionary biology is that individuals in a population differ in fitness (due to the differences in genes and/or environments experienced). Differences in fitness that have genetic bases are the most important ones because it is the changes in genes that make innovations and adaptation permanent. The relationship between genes and fitness (direct or mediated via phenotype) is obviously of fundamental importance . In the most common modern interpretation, a fitness landscape specifies a particular fitness component (e.g., viability, that is, the probability to survive to the age of reproduction) as a function defined on a particular set of genotypes or phenotypes. High-Dimensional Fitness Landscapes and Speciation 47 For example, consider a very large, randomly mating diploid population under constant viability selection. Let us focus on a particular locus with two alleles, A and a, controlling fitness (viability). Then there are three different genotypes: two homozygotes, AA and aa, and a heterozygote , Aa. An example of a fitness landscape for this simple model is given in figure 3.1a. The fitness landscape illustrated...