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.
In their classic paper, Brown and Wilson (1) proposed that mutually negative interactions 29 between closely-related species could lead to evolutionary divergence when those species co-30 occurred. In the six decades since, this idea has been debated vigorously, with support that has 31 vascillates based on the latest set of theoretical treatments and comparative studies (reviewed in 32[(2-5)]). However, tests of interaction-driven evolutionary divergence have been slow to 33 capitalize on the growing recognition that evolutionary change can occur rapidly in response to 34 strong divergent natural selection (but see [(6-9)]); thus, evolutionary hypotheses about 35 phenomena once thought to transpire on time scales too long for direct observation can be tested 36 in real time while using replicated statistical designs. 37
As range shifts coincident with climate change have become increasingly well documented, efforts to describe the causes of range boundaries have increased. Three mechanisms-genetic impoverishment, migration load, or a physical barrier to dispersal-are well described theoretically, but the data needed to distinguish among them have rarely been collected. We describe the distribution, abundance, genetic variation, and environment of Tetraclita rubescens, an intertidal barnacle that expanded its northern range limit by several hundreds of kilometres from San Francisco, CA, USA, since the 1970s. We compare geographic variation in abundance with abiotic and biotic patterns, including sea surface temperatures and the distributions of 387 co-occurring species, and describe genetic variation in cytochrome c oxidase subunit I, mitochondrial noncoding region, and nine microsatellite loci from 27 locations between Bahia Magdalena (California Baja Sur, Mexico) and Cape Mendocino (CA, USA). We find very high gene flow, high genetic diversity, and a gradient in physical environmental variation coincident with the range limit. We infer that the primary cause of the northern range boundary in T. rubescens is migration load arising from flow of maladapted alleles into peripheral locations and that environmental change, which could have reduced selection against genotypes immigrating into the newly colonized portion of the range, is the most likely cause of the observed range expansion. Because environmental change could similarly affect all taxa in a region whose distributional limits are established by migration load, these mechanisms may be common causes of range boundaries and largely synchronous multi-species range expansions.
Both scientists and the public would benefit from improved communication of basic scientific research and from integrating scientists into education outreach, but opportunities to support these efforts are limited. We have developed two low-cost programs—"Present Your PhD Thesis to a 12-Year-Old" and "Shadow a Scientist”—that combine training in science communication with outreach to area middle schools. We assessed the outcomes of these programs and found a 2-fold benefit: scientists improve their communication skills by explaining basic science research to a general audience, and students' enthusiasm for science and their scientific knowledge are increased. Here we present details about both programs, along with our assessment of them, and discuss the feasibility of exporting these programs to other universities.
The repeated evolution of similar phenotypes in independent populations (i.e. parallel or convergent evolution) provides an opportunity to identify genetic and ecological factors that influence the process of adaptation. Threespine stickleback fish ( Gasterosteus aculeatus ) are an excellent model for such studies, as they have repeatedly adapted to divergent habitats across the Northern hemisphere. Here, we use genomic, ecological and morphological data from 16 independent pairs of stickleback populations adapted to divergent lake and stream habitats. We combine a population genomic approach to identify regions of the genome that are likely under selection in these divergent habitats with an association mapping approach to identify regions of the genome that underlie variation in ecological factors and morphological traits. Over 37% of genomic windows are repeatedly differentiated across lake–stream pairs. Similarly, many genomic windows are associated with variation in abiotic factors, diet items and morphological phenotypes. Both the highly differentiated windows and candidate trait windows are non-randomly distributed across the genome and show some overlap. However, the overlap is not significant on a genome-wide scale. Together, our data suggest that adaptation to divergent food resources and predation regimes are drivers of differentiation in lake–stream stickleback, but that additional ecological factors are also important. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.
Evolutionary ecologists aim to explain and predict evolutionary change under different selective regimes. Theory suggests that such evolutionary prediction should be more difficult for biomechanical systems in which different trait combinations generate the same functional output: "many-to-one mapping." Many-to-one mapping of phenotype to function enables multiple morphological solutions to meet the same adaptive challenges. Therefore, many-to-one mapping should undermine parallel morphological evolution, and hence evolutionary predictability, even when selection pressures are shared among populations. Studying 16 replicate pairs of lake- and stream-adapted threespine stickleback (Gasterosteus aculeatus), we quantified three parts of the teleost feeding apparatus and used biomechanical models to calculate their expected functional outputs. The three feeding structures differed in their form-to-function relationship from one-to-one (lower jaw lever ratio) to increasingly many-to-one (buccal suction index, opercular 4-bar linkage). We tested for (1) weaker linear correlations between phenotype and calculated function, and (2) less parallel evolution across lake-stream pairs, in the many-to-one systems relative to the one-to-one system. We confirm both predictions, thus supporting the theoretical expectation that increasing many-to-one mapping undermines parallel evolution. Therefore, sole consideration of morphological variation within and among populations might not serve as a proxy for functional variation when multiple adaptive trait combinations exist.
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