Next-generation sequencing of pooled samples (Pool-seq) is a popular method to assess genome-wide diversity patterns in natural and experimental populations. However, Pool-seq is associated with specific sources of noise, such as unequal individual contributions. Consequently, using Pool-seq for the reconstruction of evolutionary history has remained underexplored. Here we describe a novel Approximate Bayesian Computation (ABC) method to infer demographic history, explicitly modeling Pool-seq sources of error. By jointly modeling Pool-seq data, demographic history and the effects of selection due to barrier loci, we obtain estimates of demographic history parameters accounting for technical errors associated with Pool-seq. Our ABC approach is computationally efficient as it relies on simulating subsets of loci (rather than the whole-genome), and on using relative summary statistics and relative model parameters. Our simulation study results indicate Pool-seq data allows distinction between general scenarios of ecotype formation (single versus parallel origin), and to infer relevant demographic parameters (e.g., effective sizes, split times). We exemplify the application of our method to Pool-seq data from the rocky-shore gastropod Littorina saxatilis, sampled on a narrow geographical scale at two Swedish locations where two ecotypes (Wave and Crab) are found. Our model choice and parameter estimates show that ecotypes formed before colonization of the two locations (i.e., single origin) and are maintained despite gene flow. These results indicate that demographic modeling and inference can be successful based on pool-sequencing using ABC, contributing to the development of suitable null models that allow for a better understanding of the genetic basis of divergent adaptation.

Polymorphic short insertions and deletions (INDELs ≤ 50 bp) are abundant, although less common than single nucleotide polymorphisms (SNPs). Evidence from model organisms shows INDELs to be more strongly influenced by purifying selection than SNPs. Partly for this reason, INDELs are rarely used as markers for demographic processes or to detect balancing or divergent selection. Here, we compared INDELs and SNPs in the intertidal snail Littorina saxatilis, focusing on hybrid zones between ecotypes. Using capture sequencing data, we computed INDEL and SNP site frequency spectra (SFS) to compare the impact of purifying, positive and balancing selection on these variant types. Because signatures of selection may be confounded by GC-biased gene conversion and polarization errors, we also examined their influence. We assessed the impact of divergent selection by analysing allele frequency clines across habitat boundaries. We show evidence that short INDELs are affected more by purifying selection and less by positive selection than SNPs, but part of the observed SFS difference can be attributed to GC-biased gene conversion and polarization errors. We did not find a difference in the impact of balancing or divergent selection between short INDELs and SNPs. Short INDELs and SNPs were similarly distributed across the genome and so are likely to respond to indirect selection in the same way. A few regions likely affected by divergent selection were revealed by INDELs and not by SNPs. Short INDELs can be useful genetic markers helping to identify genomic regions under selective constraints or important for adaptation and population divergence.