No abstract

Parallel evolution of similar traits by independent populations in similar environments is considered strong evidence for adaptation by natural selection. Often, however, replicate populations in similar environments do not all evolve in the same way, thus deviating from any single, predominant outcome of evolution. This variation might arise from non-adaptive, population-specific effects of genetic drift, gene flow or limited genetic variation. Alternatively, these deviations from parallel evolution might also reflect predictable adaptation to cryptic environmental heterogeneity within discrete habitat categories. Here, we show that deviations from parallel evolution are the consequence of environmental variation within habitats combined with variation in gene flow. Threespine stickleback (Gasterosteus aculeatus) in adjoining lake and stream habitats (a lake-stream 'pair') diverge phenotypically, yet the direction and magnitude of this divergence is not always fully parallel among 16 replicate pairs. We found that the multivariate direction of lake-stream morphological divergence was less parallel between pairs whose environmental differences were less parallel. Thus, environmental heterogeneity among lake-stream pairs contributes to deviations from parallel evolution. Additionally, likely genomic targets of selection were more parallel between environmentally more similar pairs. In contrast, variation in the magnitude of lake-stream divergence (independent of direction) was better explained by differences in lake-stream gene flow; pairs with greater lake-stream gene flow were less morphologically diverged. Thus, both adaptive and non-adaptive processes work concurrently to generate a continuum of parallel evolution across lake-stream stickleback population pairs.

Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations’ positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.

Although much progress has been made in identifying the genes (and, in rare cases, mutations) that contribute to phenotypic variation, less is known about the effects that these genes have on fitness. Nonetheless, genes are commonly labelled as 'adaptive' if an allele has been shown to affect a phenotype with known or suspected functional importance or if patterns of nucleotide variation at the locus are consistent with positive selection. In these cases, the 'adaptive' designation may be premature and may lead to incorrect conclusions about the relationships between gene function and fitness. Experiments to test targets and agents of natural selection within a genomic context are necessary for identifying the adaptive consequences of individual alleles.

Experimental estimates of the effects of selection on genes determining adaptive traits add to our understanding of the mechanisms of evolution. We measured selection on genotypes of the Ectodysplasin locus, which underlie differences in lateral plates in threespine stickleback fish. A derived allele (low) causing reduced plate number has been fixed repeatedly after marine stickleback colonized freshwater from the sea, where the ancestral allele (complete) predominates. We transplanted marine sticklebacks carrying both alleles to freshwater ponds and tracked genotype frequencies over a generation. The low allele increased in frequency once lateral plates developed, most likely via a growth advantage. Opposing selection at the larval stage and changing dominance for fitness throughout life suggest either that the gene affects additional traits undergoing selection or that linked loci also are affecting fitness.