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I.13 Adaptation Allan Larson OUTLINE 1. Adaptation and Darwinism 2. Adaptation as a hypothesis of evolutionary history 3. Molecular population genetics of adaptation 4. Adaptation and selfish genetic elements Darwin’s theory of natural selection explains how genetically variable populations gradually accumulate traits that enhance an organism’s ability to survive and to reproduce. Calling a particular character an adaptation denotes the hypothesis that the character arose gradually by natural selection for a particular biological role, which is called the character’s function. Any hypothesis of character adaptation is therefore a historical explanation that must specify the particular population, the interval of evolutionary time, the geographic conditions in which the relevant evolution occurred, and the nature of character variation that was sorted by natural selection. Empirical rejection of the hypothesis of character adaptation suggests the alternative hypotheses of exaptation (a character co-opted by natural selection for a biological role not associated with the character’s origin), nonaptation (a character not discriminated from alternatives by natural selection), or disaptation (a character disfavored by selection relative to alternative forms). I illustrate the contrast between adaptationist and anti-Darwinian theories of character origination using a longstanding debate concerning evolution of mimicry of wing patterns among butterfly species. I describe adaptation as a molecular population-genetic process using as an example the medical syndrome of sickle-cell anemia in African populations; depending upon its genetic and environmental contexts, hemoglobin S may constitute an exaptation , a nonaptation, a disaptation, or a component of an adaptive complex of epistatically interacting genes. Evolutionary developmental modularity and phenotypic accommodation may enhance the role of phenotypically discontinuous changes in evolution by natural selection. Selfish genetic elements likely underlie most organismal characters that arise as disaptations and nonetheless persist despite natural selection against them. Suppression of selfish genetic elements is potentially a major source of evolution by natural selection. The explicitly historical approach to adaptation illustrated here contrasts strongly with a now largely discredited analogistic approach used in older ecological literature. GLOSSARY adaptation (as a process). Evolution of a population by natural selection in which hereditary variants most favorable to organismal survival and reproduction are accumulated and less advantageous forms discarded; includes character adaptation and exaptation. balanced polymorphism. Occurrence in a population of a selective equilibrium at which two or more different allelic forms of a gene each have frequencies exceeding 0.05. character adaptation. A character that evolved gradually by natural selection for a particular biological role through which organisms possessing the character have a higher average rate of survival and reproduction than do organisms having contrasting conditions that have occurred in a population ’s evolutionary history; adaptation in this usage contrasts with disaptation, exaptation, and nonaptation . developmental constraint. A bias in the morphological forms that a population can express caused by the mechanisms and limitations of organismal growth and morphogenesis. disaptation. A character that decreases its possessors’ average rate of survival and reproduction relative to contrasting conditions evident in a population’s evolutionary history; a primary disaptation is disadvantageous within the populational context in which it first appears; a secondary disaptation acquires a selective liability not present at its origin as a consequence of environmental change or an altered genetic context. exaptation. Co-option of a character by natural selection for a biological role other than one through which the character was constructed by natural selection. function. The biological role through which an adaptive character was constructed by natural selection. gradualism. Accumulation of individually small quantitative changes in a population leads to qualitative change; contrasts with saltation, in which a single genetic change induces a large qualitative change in phenotype. mimicry. Evolution by natural selection in which a character is favored because it closely resembles one present in a different species; the species whose character is copied by a ‘‘mimic’’ is called the ‘‘model.’’ modularity. Evolution of developmental constraints by which one of two or more alternative, qualitatively different suites of characters can be activated by particular genetic or environmental cues. nonaptation. A character not selectively distinguishable from contrasting conditions present in the evolutionary history of a population. saltation. Evolution of a large, qualitative change in phenotype in a single mutational step; contrasts with gradualism. selfish genetic element. Genes that spread at a cost to the organism; stretches of DNA that act narrowly to advance their own proliferation or expression and typically cause negative effects on nonlinked genes in the same organism (modified from Burt and Trivers , 2006). 1. ADAPTATION...


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