Contrasting effects of environment and genetics generate a continuum of parallel evolution

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.

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

“…Shared outliers and/or correlated differentiation are then often interpreted as indication that divergent natural selection has targeted the same genes in multiple population pairs, and hence as evidence of parallel evolution at the molecular level. However, such analyses are frequently performed with low physical marker resolution (recent examples: Egger, Roesti, Böhne, Roth, & Salzburger, ; Perreault‐Payette et al., ; Ravinet et al., ; Raeymaekers et al., ; Rougemont et al., ; Stuart et al., ; Trucchi, Frajman, Haverkamp, Schönswetter, & Paun, ). Consequently, single markers are highly unlikely to coincide with polymorphisms under direct selection.…”

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

“…Second, when gene flow is high, spatial population divergence is often low, as shown in theory (Slatkin, ; Felsenstein, ; Kawecki, ) and empirical systems including stickleback (e.g. Hendry & Taylor, ; Stuart et al ., ).…”

Evolution and diversity of two cisco forms in an outlet of glacial Lake Algonquin

“…Divergence seems to be adaptive, yet the extent of phenotypic and genetic variation within lake is highly variable. These methods should overcome the binary grouping criterion, such as habitat of capture or nonoverlapping gill-raker distribution, that can be limiting in explaining the complexity of the phenotypic parallelism among sympatric pairs (Stuart et al, 2017). A systematic sampling design coupled with biotic and abiotic characterization including the detection of spawning grounds, differences in spawning period, or differences in trophic position would be necessary to identify and untangle the suite of factors likely influencing the extent and stages of divergence.…”