Adaptation in the age of ecological genomics: insights from parallelism and convergence

Abstract

Parallel phenotypic diversification in closely related species is a rigorous framework for testing the role of natural selection in evolution. Do parallel phenotypes always diversify by parallel genetic bases or does selection pave many alternative genomic routes to the same phenotypic ends? In this review, we show that the advent of next-generation sequencing technologies and the growing use of genomic approaches make it increasingly feasible to answer these fundamental questions using ecological and evolutionary 'non-model' populations of vertebrates in nature. While it is generally expected, and often observed, that closely related populations or species have parallel genetic bases to parallel phenotypes, exceptions are not rare and show that alternative genetic routes can result in similar phenotypes. Ultimately, this framework may illuminate the ecological conditions, evolutionary histories and genetic architectures that result in recurrent phenotypes and rapid adaptation.

Genomic tools for new insights to variation, adaptation, and evolution in the salmonid fishes: a perspective for charr

“…As genomic data can be collected more readily, the greatest gains in mining the genomics of adaptive traits will come from environment and phenotype matching, as well as increasing levels of biological replication (populations and individuals) (Elmer & Meyer, 2011;Hendry, 2013;Roesti et al, 2014). Future research will also benefit from direct and indirect functional validation, for example, the comparisons possible with the growing available genomic resources for salmonids (Pavey et al, 2012;Primmer et al, 2013).…”

“…These false positives lead us to conclude incorrectly about the genetic bases of the populations or phenotypes being studied. This is a central argument for leveraging the framework of parallel evolution (Bernatchez et al, 2010;Elmer & Meyer, 2011). Replicate Hydrobiologia (2016) 783:191-208 203 phenotypes in the parallel evolution framework are so called 'natural evolutionary experiments' (Doughty, 1996) used in comparative approaches as a way to tackle the challenges of evolutionary time scales and environmental stochasticity.…”

“…Looking for common patterns across multiple systems will allow us to distinguish true patterns from the background noise that is inherent in samples drawn from the natural environment. Therefore, this study system has the potential to tackle a fundamental and unresolved question about the extent to which there are many different genomic routes to similar phenotypic ends (Elmer & Meyer, 2011). Thus, an important question that charr as a model species will allow us to address in the future is: Do ecomorphs diverge in the same way across locations?…”

“…Across the Holarctic there are multiple and rapidly evolving divergent phenotypes (known variously as ecomorphs, morphotypes, or trophic morphs) of charr that differ in traits such as size, shape, diet, spawning time, and life history (Klemetsen, 2010;Muir et al, 2015). This high diversity is particularly informative in the context of parallel evolution of similar ecologically relevant morphologies across independent sites; such replication increases power to distinguish signal from spurious noise (Schluter, 2000;Elmer & Meyer, 2011).…”

“…in sympatry) is hypothesised to have a distinctive signature across the genome, with much of the genome having low divergence and some regions of the genome being very different between diverging populations (for review see Feder et al, 2012;Via, 2012). Discerning and disentangling such patterns in wild populations, to identify whether empirical data support theoretical predictions, is a key goal of population genomics (Butlin, 2010;Elmer & Meyer, 2011;Rice et al, 2011;Rogers et al, 2013).…”