(Non)Parallel Evolution

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

Data from: How parallel is parallel evolution? A comparative analysis in fishes

Evidence of phenotypic parallelism is often used to infer the deterministic role played by natural selection. However, variation in the extent or direction of divergence is often evident among independent evolutionary replicates, raising the following question: just how parallel, overall, is parallel evolution? We answer this question through a comparative analysis of studies of fishes, a taxon where parallel evolution has been much discussed. We first ask how much of the among-population variance in phenotypic traits can be explained by different “environment” types, such as high predation versus low predation or benthic versus limnetic. We then use phenotypic change vector analysis to quantify variation in the direction (vector angles) and magnitude (vector lengths) of environment-associated divergence. All analyses show high variation in the extent of parallelism—from very high to very low, along with everything in between—highlighting the importance of quantifying parallelism rather than just asserting its presence. Interestingly, instances of low extents of parallelism represent important components of divergence in many cases, promising considerable opportunities for inferences about the factors shaping phenotypic divergence

Ili_WR_water_depth_dryad

Habitat characteristics describing the water depth and width of each of the creek sites. Measurements include wetted width, wetted depth, and wetted depth to width ratio. All measurements are in meters. Most measurements are unavailable (NA) for beach sites

Data from: Sexual dimorphism modifies habitat‐associated divergence: Evidence from beach and creek breeding sockeye salmon

Studies of parallel or convergent evolution (the repeated, independent evolution of similar traits in similar habitats) rarely explicitly quantify the extent of parallelism (i.e., variation in the direction and/or magnitude of divergence) between the sexes; instead they often investigate both sexes together or exclude one sex. However, differences in male and female patterns of divergence could contribute to overall variation in the extent of parallelism among ecotype pairs, especially in sexually dimorphic traits. Failing to properly attribute such variation could lead to underestimates of the importance of environmental variation in shaping phenotypes. We investigate the extent of parallelism in the body shape of male and female beach and creek spawning sockeye salmon (Oncorhynchus nerka) from two lake systems in western Alaska that were colonized independently after the last ice age. Although both sexes showed some degree of parallelism, patterns of beach‐creek body shape divergence vary between the sexes and between lake systems. Phenotypic change vector analyses revealed highly parallel aspects of divergence between males from different lake systems (males from beaches had deeper bodies than males from creeks) but weaker parallelism in females, and high parallelism between the sexes in one lake system but not the other. Body shape also had population‐specific components, which were mostly, but not entirely, explained by environmental variation in the form of creek depth. Our results highlight the importance of explicitly considering the extent of parallelism between the sexes, and environmental variation among sites within habitat types

sockeye_raw_coordinates_dryad

Raw coordinate data for sockeye landmarks and curves in .tps format (from tpsDig, available at: http://life.bio.sunysb.edu/ee/rohlf/software.html). For each individual, coordinates of the 16 landmarks and two curves (25 and 15 sliders each) are provided

Clinal genomic analysis reveals strong reproductive isolation across a steep habitat transition in stickleback fish

How ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback fish population pair adapted to contiguous, ecologically different lake and stream habitats. Clinal whole-genome sequence data reveal numerous genome regions (nearly) fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center closely matches the habitat transition. Simulations confirm that such strong divergence can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from near the habitat transition before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale

Oke et al 2017 AmNat population data

Population level data for each trait. Linked to trait level data using trait identifier. Includes only those traits that met inclusion criteria

Oke et al 2017 AmNat study metadata

Information for original studies included in our analyses. All traits from all studies were not necessarily included, see article main text for inclusion criteria

Data from: Hybridization between genetically modified Atlantic salmon and wild brown trout reveals novel ecological interactions

Interspecific hybridization is a route for transgenes from genetically modified (GM) animals to invade wild populations, yet the ecological effects and potential risks that may emerge from such hybridization are unknown. Through experimental crosses, we demonstrate transmission of a growth hormone transgene via hybridization between a candidate for commercial aquaculture production, GM Atlantic salmon (Salmo salar), and closely related wild brown trout (S. trutta). Transgenic hybrids were viable and grew more rapidly than transgenic salmon and other non-transgenic crosses in hatchery-like conditions. In stream mesocosms designed to more closely emulate natural conditions, transgenic hybrids appeared to express competitive dominance and suppressed the growth of transgenic and non-transgenic (wild-type) salmon by 82% and 54%, respectively. To the best of our knowledge, this is the first demonstration of environmental impacts of hybridization between a GM animal and a closely related species. These results provide empirical evidence of the first steps towards introgression of foreign transgenes into the genomes of new species and contribute to the growing evidence that transgenic animals have complex and context-specific interactions with wild populations. We suggest that interspecific hybridization be explicitly considered when assessing the environmental consequences should transgenic animals escape to nature