Abstract
BackgroundSalmonid fishes are characterised by a very high level of variation in trophic, ecological, physiological, and life history adaptations. Some salmonid taxa show exceptional potential for fast, within-lake diversification into morphologically and ecologically distinct variants, often in parallel; these are the lake-resident charr and whitefish (several species in the genera Salvelinus and Coregonus). To identify selection on genes and gene categories associated with such predictable diversifications, we analysed 2702 orthogroups (4.82 Mbp total; average 4.77 genes/orthogroup; average 1783 bp/orthogroup). We did so in two charr and two whitefish species and compared to five other salmonid lineages, which do not evolve in such ecologically predictable ways, and one non-salmonid outgroup.ResultsAll selection analyses are based on Coregonus and Salvelinus compared to non-diversifying taxa. We found more orthogroups were affected by relaxed selection than intensified selection. Of those, 122 were under significant relaxed selection, with trends of an overrepresentation of serine family amino acid metabolism and transcriptional regulation, and significant enrichment of behaviour-associated gene functions. Seventy-eight orthogroups were under significant intensified selection and were enriched for signalling process and transcriptional regulation gene ontology terms and actin filament and lipid metabolism gene sets. Ninety-two orthogroups were under diversifying/positive selection. These were enriched for signal transduction, transmembrane transport, and pyruvate metabolism gene ontology terms and often contained genes involved in transcriptional regulation and development. Several orthogroups showed signs of multiple types of selection. For example, orthogroups under relaxed and diversifying selection contained genes such as ap1m2, involved in immunity and development, and slc6a8, playing an important role in muscle and brain creatine uptake. Orthogroups under intensified and diversifying selection were also found, such as genes syn3, with a role in neural processes, and ctsk, involved in bone remodelling.ConclusionsOur approach pinpointed relevant genomic targets by distinguishing among different kinds of selection. We found that relaxed, intensified, and diversifying selection affect orthogroups and gene functions of ecological relevance in salmonids. Because they were found consistently and robustly across charr and whitefish and not other salmonid lineages, we propose these genes have a potential role in the replicated ecological diversifications.
Highlights
Salmonid fishes are characterised by a very high level of variation in trophic, ecological, physiological, and life history adaptations
Orthogroups with signals of diversifying selection showed a clear trend towards enrichment for signal transduction, transmembrane transport, proteolysis, lipid metabolism, and pyruvate metabolism gene ontology (GO) terms (Fig. 4, Table 1) and often contained genes involved in transcriptional regulation, development, lipid metabolism, and immunity
Our findings suggest that there is some evidence for a parallel relaxation of selective constraint in the repeatedly diversifying salmonid lineages Coregonus and Salvelinus compared to all other salmonid lineages, which are known to be less diversifying
Summary
Salmonid fishes are characterised by a very high level of variation in trophic, ecological, physiological, and life history adaptations. Some salmonid taxa show exceptional potential for fast, within-lake diversification into morphologically and ecologically distinct variants, often in parallel; these are the lake-resident charr and whitefish (several species in the genera Salvelinus and Coregonus). Ecological opportunity differs dramatically among cichlid lineages [23,24,25,26,27], which makes it difficult to pinpoint taxa in which adaptive potential is elevated due to a shared genetic toolset [3, 6]. Freshwater lake-resident salmonids of different species and genera have similar ecological opportunity and commonly sympatric distributions across the northern hemisphere [28,29,30]. The freshwater habitats of northern fishes were all colonised on a similar postglacial timescale [30, 31], unlike the dramatically different and complex colonisation histories of cichlids [4, 32,33,34]
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