Abstract

Adaptive genetic variation is a function of both selective and neutral forces. To accurately identify adaptive loci, it is thus critical to account for demographic history. Theory suggests that signatures of selection can be inferred using the coalescent, following the premise that genealogies of selected loci deviate from neutral expectations. Here, we build on this theory to develop an analytical framework to identify loci under selection via explicit demographic models (LSD). Under this framework, signatures of selection are inferred through deviations in demographic parameters, rather than through summary statistics directly, and demographic history is accounted for explicitly. Leveraging the property of demographic models to incorporate directionality, we show that LSD can provide information on the environment in which selection acts on a population. This can prove useful in elucidating the selective processes underlying local adaptation, by characterizing genetic trade‐offs and extending the concepts of antagonistic pleiotropy and conditional neutrality from ecological theory to practical application in genomic data. We implement LSD via approximate Bayesian computation and demonstrate, via simulations, that LSD (a) has high power to identify selected loci across a large range of demographic‐selection regimes, (b) outperforms commonly applied genome‐scan methods under complex demographies and (c) accurately infers the directionality of selection for identified candidates. Using the same simulations, we further characterize the behaviour of isolation‐with‐migration models conducive to the study of local adaptation under regimes of selection. Finally, we demonstrate an application of LSD by detecting loci and characterizing genetic trade‐offs underlying flower colour in Antirrhinum majus.

Highlights

  • Elucidating the genetic basis of adaptation and identifying genetic determinants of population and species divergence are key foci in evolutionary biology

  • We evaluated the performance of our LSD implementation at identifying selected loci under these simulations by plotting the true positive rate (TPR) against the false positive rate (FPR) under the choice of highest posterior density interval (HPDI) thresholds from 0 to 1, and reporting the area under the curve (AUC) of the resultant receiver operating characteristic (ROC) curve

  • While LSD is flexible regarding the choice of demographic models employed and can be applied to single and multiple populations, we focus here on processes that lead to selection against gene flow, namely local adaptation and extrinsic reproductive barriers, that can be inferred via their expectation to reduce ME

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Summary

| INTRODUCTION

Elucidating the genetic basis of adaptation and identifying genetic determinants of population and species divergence are key foci in evolutionary biology. There exists only a single likelihood implementation to infer locus-­specific and global demographic parameters jointly: an Markov chain Monte Carlo (MCMC) sampler that attributes loci to different classes (e.g., selected and neutral) and jointly infers the demographic parameters of a two-­population isolation-­with-­migration (IM) model for each group (Sousa et al, 2013) To extend this approach to more complex models, simulation-­ based techniques such as approximate Bayesian computation (ABC) (Beaumont et al, 2002; Marjoram & Tavaré, 2006; Sisson et al, 2018) may be employed. We validate and assess the performance of LSD via extensive simulations, provide general insights into the properties of IM models in relation to the power of LSD and other widely applied genome scan methods, and demonstrate an application of the method to the detection of functionally validated loci underlying flower colour in two parapatric subspecies of Antirrhinum majus (common snapdragon) (Schwinn et al, 2006; Tavares et al, 2018)

| MATERIALS AND METHODS
| RESULTS
| DISCUSSION
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