Gene Flow and Habitat Heterogeneity Shape Coexistence Dynamics of Arctic Charr Morphs in Connected Lakes

Abstract

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-charr 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 hybridisation between PI- and LB-charr in both lakes. Moreover, the higher hybridisation 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.