Sympatric morphs provide valuable systems for studying incipient divergence despite incomplete reproductive isolation. In connected waterbodies with spatially heterogeneous habitats, one or more morphs may form metapopulation structures, generating eco-evolutionary dynamics unlike those in single lakes. We studied the phenotypic and genome-wide differentiation in Arctic charr (Salvelinus alpinus) in two Icelandic lakes: Thingvallavatn, known to harbour four distinct morphs, and a smaller downstream lake, Ulfljotsvatn. Our analyses confirm a single origin of charr polymorphism in this system, with all morphs present in both lakes. Relative morph abundances differ between the lakes: PL-charr dominate in Thingvallavatn, whereas LB-charr are most abundant in Ulfljotsvatn. Three morphs, large- (LB-), small (SB-) benthivorous and planktivorous (PL-) charr, are genetically distinct. The system likely forms a source-sink structure for both PL- and SB-charr, though migration rates from Thingvallavatn vary remarkably, resulting in distinct population dynamics. Conversely, LB-char exhibit genetic differentiation between the lakes, suggesting the presence of a separate population in Ulfljotsvatn. While piscivorous (PI-) charr appear genetically similar to PL-charr, evidence suggests hybridization between PI- and LB-charr in both lakes. Moreover, the higher hybridization in the downstream lake likely contributes to the observed erosion of genetic separation between LB- and PL-charr in Ulfljotsvatn. These findings suggest that the complex interplay of habitat heterogeneity and morph-specific migrations shapes the coexistence and eco-evolutionary dynamics of sympatric charr morphs in the connected lakes. Our study highlights the importance of investigating early divergence in spatially complex systems to advance eco-evolutionary research.

Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole-genome-sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defense traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high (h2 = 0.42 – 0.65), indicating adaptive potential for all traits. Whilst environment-association analyses identified thousands of loci putatively involved in selection, related to genes linked to neuron development and protein phosphorylation, only allelic variation linked to pelvic spine length was concurrently linked to environmental variation (water depth) - supporting the conclusion that divergence in pelvic spine length occurred in face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics.