Whole‐genome sequencing illuminates multifaceted targets of selection to humic substances in Eurasian perch

Abstract

Extreme environments are inhospitable to the majority of species, but some organisms are able to survive in such hostile conditions due to evolutionary adaptations. For example, modern bony fishes have colonized various aquatic environments, including perpetually dark, hypoxic, hypersaline and toxic habitats. Eurasian perch (Perca fluviatilis) is among the few fish species of northern latitudes that is able to live in very acidic humic lakes. Such lakes represent almost “nocturnal” environments; they contain high levels of dissolved organic matter, which in addition to creating a challenging visual environment, also affects a large number of other habitat parameters and biotic interactions. To reveal the genomic targets of humic‐associated selection, we performed whole‐genome sequencing of perch originating from 16 humic and 16 clear‐water lakes in northern Europe. We identified over 800,000 single nucleotide polymorphisms, of which >10,000 were identified as potential candidates under selection (associated with >3000 genes) using multiple outlier approaches. Our findings suggest that adaptation to the humic environment may involve hundreds of regions scattered across the genome. Putative signals of adaptation were detected in genes and gene families with diverse functions, including organism development and ion transportation. The observed excess of variants under selection in regulatory regions highlights the importance of adaptive evolution via regulatory elements, rather than via protein sequence modification. Our study demonstrates the power of whole‐genome analysis to illuminate the multifaceted nature of humic adaptation and provides the foundation for further investigation of causal mutations underlying phenotypic traits of ecological and evolutionary importance.

Unlocking the genome of perch – From genes to ecology and back again

“…1060 times more continuous, 4.5 times less fragmented and nearly two times more complete perch genome assembly (Ozerov et al, 2018; scaffold N50 = 6.3 Mb, BUSCO completeness of 87.6%). This has served as a backbone in several studies on perch adaptation and transcriptome activity (e.g., Jiang et al, 2022; Noreikiene et al, 2020; Ozerov et al, 2022). Finally, in 2020 a very high‐quality chromosome‐level assembly of perch (scaffold N50 = 39.6 Mb, BUSCO completeness of 97.6%), generated using long‐reads technology (Roques et al, 2020), became publicly available.…”

“…For further consideration, the study of Ozerov et al (2022) demonstrates the multifaceted nature of humic-driven selection and the power of whole-genome analysis to pinpoint genomic regions and the specific genes involved in adaptation to specific environments.…”

“…Yet, most traits are complex in nature and influenced by the environment and a large number of genes, each with a small effect (Boyle et al, 2017). In perch, the genome-wide quests for selective sweeps are just beginning to emerge, assisted by the availability of annotated whole-genome assembly (Ozerov et al, 2022, Case study 1).…”

“…In turn, access to the reference genome assembly has helped to discover hundreds of thousands of SNPs in perch (Ozerov et al, 2022) and fuelled the development of the Axiom SNP array platform (MultiFishSNPChip_1.0) which consists of nearly 4000 SNPs (Figure 3). The SNPs included in this array are distributed along 24 chromosomes (Figure 3a) and consist of both neutral, as well as putatively selected variants identified earlier (Ozerov et al, 2022; Figure 3b). To illustrate the power of the SNPs to resolve genetic relationships among populations, we genotyped 42 individual perch collected from 21 lakes in five countries (Figure 3d,e).…”

Subtle transcriptomic response of Eurasian perch (Perca fluvatilis) associated with Triaenophorus nodulosus plerocercoid infection

“…It is a generalist feeder and has a rich parasite fauna [14][15][16][17] hosting nearly 150 parasite species [13]. Despite a large and increasing body of research on perch biology, ecology, and genetics [18][19][20], relatively little is known about perch-parasite interactions at a molecular level [20]; however, this situation is slowly changing, at least in part because of growing importance of Eurasian perch in aquaculture [21] and an increasing availability of molecular resources [22][23][24]. Yet, the ecological relevance of the majority of parasite infections on perch are currently not known, which underlines the need for performing studies outside of a contained laboratory settings [25].…”