Abstract

A major goal of molecular evolutionary biology is to identify loci or regions of the genome under selection versus those evolving in a neutral manner. Correct identification allows accurate inference of the evolutionary process and thus comprehension of historical and contemporary processes driving phenotypic change and adaptation. A fundamental difficulty lies in distinguishing sites targeted by selection from both sites linked to these targets and sites fully independent of selection. These three categories of sites necessitate attention in light of the debate over the relative importance of selection versus neutrality and the neutral theory. Modern genomic insights have proved that complex processes such as linkage, demography, and biased gene conversion complicate our understanding of the role of neutral versus selective processes in evolution. In this perspective, we first highlight the importance of the genomic and (a)biotic context of new mutations to identify the targets of natural selection. We then present mechanisms that may constrain the evolution of genomes and bias the inference of selection. We discuss these mechanisms within the two critical levels that they occur: the population level and the molecular level. We highlight that they should be taken into account to correctly distinguish sites across the genome subject to selective or non-selective forces and stress that a major current field-wide goal is to quantify the absolute importance of these mechanisms.

Highlights

  • Genomic and environmental contextThe context in which mutations occur plays an important role in the actions of selection versus drift

  • Galtier and Duret, 2007; Pollard et al, 2006), or inference of the distribution of fitness effects (DFE). Though these are few examples, we argue that these population and molecular processes are prevalent enough to act as major determinants of genomic diversity and are easy to confound with selection

  • Identifying a variant as subject to natural selection is difficult since the selective environment of an allele is a combination of its own innate properties impacting the genome, along with epistatic effects due to its genomic environment, as well as its demographic situation, and lastly its (a)biotic environment

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Summary

Genomic and environmental context

The context in which mutations occur plays an important role in the actions of selection versus drift. Hill-Robertson interference may complicate identifying both the presence of selection and the sites it targets All of these effects depend on many parameters, for instance, with a single population undergoing partial self-fertilization, selective interference on deleterious alleles tends to reduce mean fitness and increase inbreeding depression. We argue that even if some cases of demographic processes may be versions of genetic drift, in that they are due to sampling process, the signatures that they leave in populations differs from that of single, ideal populations undergoing drift, emphasizing their importance in distinguishing selection from neutrality We define these as non-adaptive processes since they are neither the direct action of selection nor are they purely subject to drift (Table 1). Spatial expansion (gene surfing) yes yes Strong genetic drift over space, can mimic selection

Background selection
Population-level processes
Molecular-level processes
Background selection Associative overdominance
Conclusion
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