Department Fish Ecology and Evolution

Genomic diversity is associated with the adaptive potential of a population and thereby impacts the extinction risk of a species during environmental change. However, empirical data on genomic diversity of populations before environmental perturbations are rare and hence our understanding of the impact of perturbation on diversity is often limited. We here assess genomic diversity utilising whole-genome resequencing data from all four species of the Lake Constance Alpine whitefish radiation. Our data covers a period of strong but transient anthropogenic environmental change and permits us to track changes in genomic diversity in all species over time. Genomic diversity became strongly reduced during the period of anthropogenic disturbance and has not recovered yet. The decrease in genomic diversity varies between 18% and 30%, depending on the species. Interspecific allele frequency differences of SNPs located in potentially ecologically relevant genes were homogenized over time. This suggests that in addition to the reduction of genome-wide genetic variation, the differentiation that evolved in the process of adaptation to alternative ecologies between species might have been lost during the ecological disturbance. The erosion of substantial amounts of genomic variation within just a few generations in combination with the loss of potentially adaptive genomic differentiation, both of which had evolved over thousands of years, demonstrates the sensitivity of biodiversity in evolutionary young adaptive radiations towards environmental disturbance. Natural history collections, such as the one used for this study, are instrumental in the assessment of genomic consequences of anthropogenic environmental change. Historical samples enable us to document biodiversity loss against the shifting baseline syndrome and advance our understanding of the need for efficient biodiversity conservation on a global scale.

Anthropogenic disturbances of ecosystems are causing a loss of biodiversity at an unprecedented rate. Species extinctions often leave ecological niches underutilized, and their colonization by other species may require new adaptation. In Lake Constance, on the borders of Germany, Austria and Switzerland, an endemic profundal whitefish species went extinct during a period of anthropogenic eutrophication. In the process of extinction, the deep-water species hybridized with three surviving whitefish species of Lake Constance, resulting in introgression of genetic variation that is potentially adaptive in deep-water habitats. Here, we sampled a water depth gradient across a known spawning ground of one of these surviving species, Coregonus macrophthalmus, and caught spawning individuals at greater depths (down to 90 m) than historically recorded. We sequenced a total of 96 whole genomes, 11-17 for each of six different spawning depth populations (4, 12, 20, 40, 60 and 90 m), to document genomic intraspecific differentiation along a water depth gradient. We identified 52 genomic regions that are potentially under divergent selection between the deepest (90 m) and all shallower (4-60 m) spawning habitats. At 12 (23.1%) of these 52 loci, the allele frequency pattern across historical and contemporary populations suggests that introgression from the extinct species potentially facilitates ongoing adaptation to deep water. Our results are consistent with the syngameon hypothesis, proposing that hybridization between members of an adaptive radiation can promote further niche expansion and diversification. Furthermore, our findings demonstrate that introgression from extinct into extant species can be a source of evolvability, enabling rapid adaptation to environmental change, and may contribute to the ecological recovery of ecosystem functions after extinctions.

Adaptive radiations represent some of the most remarkable explosions of diversification across the tree of life. However, the constraints to rapid diversification and how they are sometimes overcome, particularly the relative roles of genetic architecture and hybridization, remain unclear. Here, we address these questions in the Alpine whitefish radiation, using a whole-genome dataset that includes multiple individuals of each of the 22 species belonging to six ecologically distinct ecomorph classes across several lake-systems. We reveal that repeated ecological and morphological diversification along a common environmental axis is associated with both genome-wide allele frequency shifts and a specific, larger effect, locus, associated with the gene edar. Additionally, we highlight the possible role of introgression between species from different lake-systems in facilitating the evolution and persistence of species with unique trait combinations and ecology. These results highlight the importance of both genome architecture and secondary contact with hybridization in fuelling adaptive radiation.

Salmonids are of particular interest to evolutionary biologists due to their incredible diversity of life-history strategies and the speed at which many salmonid species have diversified. In Switzerland alone, over 30 species of Alpine whitefish from the subfamily Coregoninae have evolved since the last glacial maximum, with species exhibiting a diverse range of morphological and behavioural phenotypes. This, combined with the whole genome duplication which occurred in the ancestor of all salmonids, makes the Alpine whitefish radiation a particularly interesting system in which to study the genetic basis of adaptation and speciation and the impacts of ploidy changes and subsequent rediploidization on genome evolution. Although well curated genome assemblies exist for many species within Salmonidae, genomic resources for the subfamily Coregoninae are lacking. To assemble a whitefish reference genome, we carried out PacBio sequencing from one wild-caught Coregonus sp. "Balchen" from Lake Thun to ~90x coverage. PacBio reads were assembled independently using three different assemblers, Falcon, Canu and wtdbg2 and subsequently scaffolded with additional Hi-C data. All three assemblies were highly contiguous, had strong synteny to a previously published Coregonus linkage map, and when mapping additional short-read data to each of the assemblies, coverage was fairly even across most chromosome-scale scaffolds. Here, we present the first de novo genome assembly for the Salmonid subfamily Coregoninae. The final 2.2 Gb wtdbg2 assembly included 40 scaffolds, an N50 of 51.9 Mb, and was 93.3% complete for BUSCOs. The assembly consisted of ~52% TEs and contained 44,525 genes.

Ecosystem degradation and biodiversity loss are major global challenges. When reproductive isolation between species is contingent on the interaction of intrinsic lineage traits with features of the environment, environmental change can weaken reproductive isolation and result in extinction through hybridization. By this process called speciation reversal, extinct species can leave traces in genomes of extant species through introgressive hybridization. Using historical and contemporary samples, we sequenced all four species of an Alpine whitefish radiation before and after anthropogenic lake eutrophication and the associated loss of one species through speciation reversal. Despite the extinction of this taxon, substantial fractions of its genome, including regions shaped by positive selection before eutrophication, persist within surviving species as a consequence of introgressive hybridization during eutrophication. Given the prevalence of environmental change, studying speciation reversal and its genomic consequences provides fundamental insights into evolutionary processes and informs biodiversity conservation.

The erosion of habitat heterogeneity can reduce species diversity directly but can also lead to the loss of distinctiveness of sympatric species through speciation reversal. We know little about changes in genomic differentiation during the early stages of these processes, which can be mediated by anthropogenic perturbation. Here, we analyse three sympatric whitefish species (Coregonus spp) sampled across two neighbouring and connected Swiss pre‐alpine lakes, which have been differentially affected by anthropogenic eutrophication. Our data set comprises 16,173 loci genotyped across 138 whitefish using restriction‐site associated DNA sequencing (RADseq). Our analysis suggests that in each of the two lakes the population of a different, but ecologically similar, whitefish species declined following a recent period of eutrophication. Genomic signatures consistent with hybridisation are more pronounced in the more severely impacted lake. Comparisons between sympatric pairs of whitefish species with contrasting ecology, where one is shallow benthic and the other one more profundal pelagic, reveal genomic differentiation that is largely correlated along the genome, while differentiation is uncorrelated between pairs of allopatric provenance with similar ecology. We identify four genomic loci that provide evidence of parallel divergent adaptation between the shallow benthic species and the two different more profundal species. Functional annotations available for two of those loci are consistent with divergent ecological adaptation. Our genomic analysis indicates the action of divergent natural selection between sympatric whitefish species in pre‐alpine lakes and reveals the vulnerability of these species to anthropogenic alterations of the environment and associated adaptive landscape.

Genomic datasets continue to increase in number due to the ease of production for a wider selection of species including non-model organisms. For many of these species, especially those with large or polyploid genomes, highly contiguous and well-annotated genomes are still rare due to the complexity and cost involved in their assembly. As a result, a common starting point for genomic work in non-model species is the production of a linkage map. Dense linkage maps facilitate the analysis of genomic data in a variety of ways, from broad scale observations regarding genome structure e.g. chromosome number and type or sex-related structural differences, to fine scale patterns e.g. recombination rate variation and co-localization of differentiated regions. Here we present both sex-averaged and sex-specific linkage maps for Coregonus sp. "Albock", a member of the European whitefish lineage (C. lavaretus spp. complex), containing 5395 single nucleotide polymorphism (SNP) loci across 40 linkage groups to facilitate future investigation into the genomic basis of whitefish adaptation and speciation. The map was produced using restriction-site associated digestion (RAD) sequencing data from two wild-caught parents and 156 F1 offspring. We discuss the differences between our sex-averaged and sex-specific maps and identify genome-wide synteny between C. sp. "Albock" and Atlantic Salmon (Salmo salar), which have diverged following the salmonid-specific whole genome duplication. Our analysis confirms that many patterns of synteny observed between Atlantic Salmon and Oncorhynchus and Salvelinus species are also shared by members of the Coregoninae subfamily. We also show that regions known for their species-specific rediploidization history can pose challenges for synteny identification since these regions have diverged independently in each salmonid species following the salmonid-specific whole genome duplication. The European whitefish map provided here will enable future studies to understand the distribution of loci of interest, e.g. F_ST outliers, along the whitefish genome as well as assisting with the de novo assembly of a whitefish reference genome.