Abstract
Over the past four decades, the predominant view of molecular evolution saw little connection between natural selection and genome evolution, assuming that the functionally constrained fraction of the genome is relatively small and that adaptation is sufficiently infrequent to play little role in shaping patterns of variation within and even between species. Recent evidence from Drosophila, reviewed here, suggests that this view may be invalid. Analyses of genetic variation within and between species reveal that much of the Drosophila genome is under purifying selection, and thus of functional importance, and that a large fraction of coding and noncoding differences between species are adaptive. The findings further indicate that, in Drosophila, adaptations may be both common and strong enough that the fate of neutral mutations depends on their chance linkage to adaptive mutations as much as on the vagaries of genetic drift. The emerging evidence has implications for a wide variety of fields, from conservation genetics to bioinformatics, and presents challenges to modelers and experimentalists alike.
Highlights
We have known for over half a century that the genome encodes the heritable phenotypes of an organism and that this genetic information is maintained and modified by natural selection on randomly arising mutations
We still know remarkably little about the genetic basis of phenotypic evolution or about how the selective pressures on phenotypes are reflected in genome evolution
How many sites in the genome encode functions that are maintained by natural selection? How many changes underlie adaptations and how often do such adaptive changes occur? Are adaptive changes clustered in genomic regions associated with particular functions or even in particular genes or are they dispersed throughout the genome? Do adaptive changes tend to occur in coding regions or in regulatory elements? Do most adaptive changes have substantial effects on the fitness of the organism or represent mere ‘‘fine tunings?’’
Summary
We have known for over half a century that the genome encodes the heritable phenotypes of an organism and that this genetic information is maintained and modified by natural selection on randomly arising mutations. Because purifying selection on synonymous sites reduces divergence more than polymorphism, it can cause an over-estimate of the fraction of adaptive amino acid substitutions, a [48].
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