Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

Abstract

The availability of diverse ecological niches can promote adaptation of trophic specializations and related traits, as has been repeatedly observed in evolutionary radiations of freshwater fish. The role of genetics, environment, and history in ecologically driven divergence and adaptation, can be studied on adaptive radiations or populations showing ecological polymorphism. Salmonids, especially the Salvelinus genus, are renowned for both phenotypic diversity and polymorphism. Arctic charr (Salvelinus alpinus) invaded Icelandic streams during the glacial retreat (about 10,000 years ago) and exhibits many instances of sympatric polymorphism. Particularly, well studied are the four morphs in Lake Þingvallavatn in Iceland. The small benthic (SB), large benthic (LB), planktivorous (PL), and piscivorous (PI) charr differ in many regards, including size, form, and life history traits. To investigate relatedness and genomic differentiation between morphs, we identified variable sites from RNA‐sequencing data from three of those morphs and verified 22 variants in population samples. The data reveal genetic differences between the morphs, with the two benthic morphs being more similar and the PL‐charr more genetically different. The markers with high differentiation map to all linkage groups, suggesting ancient and pervasive genetic separation of these three morphs. Furthermore, GO analyses suggest differences in collagen metabolism, odontogenesis, and sensory systems between PL‐charr and the benthic morphs. Genotyping in population samples from all four morphs confirms the genetic separation and indicates that the PI‐charr are less genetically distinct than the other three morphs. The genetic separation of the other three morphs indicates certain degree of reproductive isolation. The extent of gene flow between the morphs and the nature of reproductive barriers between them remain to be elucidated.

Limited genetic parallelism underlies recent, repeated incipient speciation in geographically proximate populations of an Arctic fish (Salvelinus alpinus)

“…Like all salmonids, the species has recently undergone a whole genome duplication ~88 Ma (Macqueen & Johnston, 2014) and therefore constitutes an ideal model for studying genomic parallelism. Studies investigating the genetic differentiation among sympatric Arctic Charr morphs (e.g., Gíslason et al., 1999; Gomez‐Uchida et al., 2008; Gordeeva et al., 2015) examined sympatric morphs using a few neutral markers and only within landlocked populations (i.e., populations residing in lakes which are separated from the sea by a physical barrier preventing migration) (but see Guðbrandsson et al., 2019; Jacobs et al., 2020). Therefore, the adaptive differentiation among morphs in sea accessible environments, where anadromous and resident individuals may coexist, and the degree to which such adaptive differentiation exhibits evidence of parallelism is largely unexplored in this species.…”

Otolith-based discrimination of cod ecotypes and the effect of growth rate

“…Similar intra-lake divergence has been noted in lake trout ( Salvelinus namaychus ), where ecotypes have developed independently in separate lake populations [55]. Perhaps the clearest example of ecotype development is found in Arctic char ( Salvelinus alpinus ) in Þingvallavatn (Iceland), where significantly divergent ecotypes have developed rapidly in the last 10,000 years, offering an opportunity to study speciation [4, 54, 55, 56, 57]. While the clear morphological differences between the Arctic char ecotypes make them readily distinguishable, the identification of ecotypes in other species can be more complicated, as is the case for cod in the present study.…”

“…where significantly divergent ecotypes have developed rapidly in the last 10,000 years, offering an opportunity to study speciation [4,54,55,56,57]. While the clear morphological differences between the Arctic char ecotypes make them readily distinguishable, the identification of ecotypes in other species can be more complicated, as is the case for cod in the present study.…”

The effect of growth rate on otolith-based discrimination of cod (Gadus morhua) ecotypes

“…The most striking ecotype examples in fish are found in freshwater, where substantial phenotypic and genetic divergence has taken place since the end of the last glacial period. Perhaps the clearest example of ecotype development is found in Arctic char ( Salvelinus alpinus ) in Þingvallavatn (Iceland), where significantly divergent ecotypes have developed rapidly in the last 10,000 years, offering an opportunity to study speciation [ 5 , 56 – 58 ]. While the clear morphological differences between the Arctic char ecotypes make them readily distinguishable, the identification of ecotypes in other species can be more complicated, as is the case for cod in the present study.…”