The repeated occurrence of similar phenotypes in independent lineages (i.e., parallel evolution) in response to similar ecological conditions can provide compelling insights into the process of adaptive evolution. An intriguing question is to what extent repeated phenotypic changes are underlain by repeated changes at the genomic level and whether patterns of genomic divergence differ with the geographic context in which populations evolve. Here, we combine genomic, morphological and ecological datasets to investigate the genomic signatures of divergence across populations of threespine stickleback (Gasterosteus aculeatus) that adapted to contrasting trophic niches (benthic or limnetic) in either sympatry or allopatry. We found that genome-wide differentiation (FST) was an order of magnitude higher and substantially more repeatable for sympatric benthic and limnetic specialists compared to allopatric populations with similar levels of trophic divergence. We identified 55 genomic regions consistently differentiated between sympatric ecotypes that were also associated with benthic vs. limnetic niche across allopatric populations. These candidate regions were enriched on three chromosomes known to be involved in the benthic-limnetic divergence of threespine stickleback. Some candidate regions overlapped with QTL for body shape and trophic traits such as number of gill rakers, traits that strongly differ between benthic and limnetic ecotypes. In sum, our study shows that magnitude and repeatability of genomic signatures of trophic divergence in threespine stickleback highly depend on the geographical context. The identified candidate regions provide starting points to identify functionally important genes for the adaptation to benthic and limnetic trophic niches.

Major Histocompatibility Complex (MHC) genes encode for proteins that recognize foreign protein antigens to initiate T-cell mediated adaptive immune responses. They are often the most polymorphic genes in vertebrate genomes. How evolution maintains this diversity is still an unsettled issue. Three main hypotheses seek to explain the maintenance of MHC diversity by invoking pathogen-mediated selection: heterozygote advantage, frequency-dependent selection, and fluctuating selection across landscapes or through time. Here, we use a large-scale field parasite survey in a stickleback metapopulation to test predictions derived from each of these hypotheses. We identify over a thousand MHCIIβ alleles and find that many of them covary positively or negatively with parasite load, suggesting that these genes contribute to resistance or susceptibility. However, despite our large sample-size, we find no evidence for the widely-cited stabilizing selection on MHC heterozygosity, in which individuals with an intermediate number of MHC alleles have the lowest parasite burden. Nor do we observe a rare-allele advantage, or widespread fluctuating selection across populations. In contrast, we find that MHC diversity is best predicted by neutral genome-wide heterozygosity and between-population genomic divergence, suggesting neutral processes are important in shaping the pattern of metapopulation MHC diversity. Thus, although MHCIIβ is highly diverse and relevant to the type and intensity of macroparasite infection in these populations of stickleback, the main models of MHC evolution still provide little explanatory power in this system.