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.

Human activities have facilitated the invasion of freshwater ecosystems by various organisms. Especially, invasive bivalves such as the quagga mussels, Dreissena bugensis, have the potential to alter ecosystem function as they heavily affect the food web. Quagga mussels occur in high abundance, have a high filtration rate, quickly spread within and between waterbodies via pelagic larvae, and colonize various substrates. They have invaded various waterbodies across the Northern Hemisphere. In Central Europe, they have invaded multiple large and deep perialpine lakes with first recordings in Lake Geneva in 2015 and 2016 in Lake Constance. In the deep perialpine lakes, quagga mussels quickly colonized the littoral zone but are also abundant deeper (>80 m), where they are often thinner and brighter shelled. We analysed 675 quagga mussels using ddRAD sequencing to gain in-depth insights into the genetic population structure of quagga mussels across Central European lakes and across various sites and depth habitats in Lake Constance. We revealed substantial genetic differentiation amongst quagga mussel populations from three unconnected lakes, and all populations showed high genetic diversity and effective population size. In Lake Constance, we detected no genetic differentiation amongst quagga mussels sampled across different sites and depth habitats. We also did not identify any convincing candidate loci evidential for adaptation along a depth gradient and a transplant experiment showed no indications of local adaptation to living in the deep based on investigating growth and survival. Hence, the shallow-water and the deep-water morphotypes seem to be a result of phenotypic plasticity rather than local adaptation to depth. In conclusion, our ddRAD approach revealed insight into the establishment of genetically distinct quagga mussel populations in three perialpine lakes and suggests that phenotypic plasticity and life history traits (broadcast spawner with high fecundity and dispersing pelagic larvae) facilitate the fast spread and colonization of various depth habitats by the quagga mussel.

Host–parasite interactions can cause strong demographic fluctuations accompanied by selective sweeps of resistance/infectivity alleles. Both demographic bottlenecks and frequent sweeps are expected to reduce the amount of segregating genetic variation and therefore might constrain adaptation during co-evolution. Recent studies, however, suggest that the interaction of demographic and selective processes is a key component of co-evolutionary dynamics and may rather positively affect levels of genetic diversity available for adaptation. Here, we provide direct experimental testing of this hypothesis by disentangling the effects of demography, selection and their interaction in an experimental host–parasite system. We grew 12 populations of a unicellular, asexually reproducing algae (Chlorella variabilis) that experienced either growth followed by constant population sizes (three populations), demographic fluctuations (three populations), selection induced by exposure to a virus (three populations), or demographic fluctuations together with virus-induced selection (three populations). After 50 days (~50 generations), we conducted whole-genome sequencing of each algal host population. We observed more genetic diversity in populations that jointly experienced selection and demographic fluctuations than in populations where these processes were experimentally separated. In addition, in those three populations that jointly experienced selection and demographic fluctuations, experimentally measured diversity exceeds expected values of diversity that account for the cultures' population sizes. Our results suggest that eco-evolutionary feedbacks can positively affect genetic diversity and provide the necessary empirical measures to guide further improvements of theoretical models of adaptation during host–parasite co-evolution.

Speciation research—the scientific field focused on understanding the origin and diversity of species—has a long and complex history. While relevant to one another, the specific goals and activities of speciation researchers are highly diverse, and scattered across a collection of different perspectives. Thus, our understanding of speciation will benefit from efforts to bridge scientific findings and the diverse people who do the work. In this paper, we outline two ways of integrating speciation research: (i) scientific integration, through the bringing together of ideas, data, and approaches; and (ii) social integration, by creating ways for a diversity of researchers to participate in the scientific process. We then discuss five challenges to integration: (i) the multidisciplinary nature of speciation research, (ii) the complex language of speciation; (iii) a bias toward certain study systems; (iv) the challenges of working across scales; and (v) inconsistent measures and reporting standards. We provide practical steps that individuals and groups can take to help overcome these challenges, and argue that integration is a team effort in which we all have a role to play.

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.

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.

Characterizing how viruses evolve expands our understanding of the underlying fundamental processes, such as mutation, selection and drift. One group of viruses whose evolution has not yet been extensively studied are the Phycodnaviridae, a globally abundant family of aquatic large dsDNA viruses. Here we studied the evolutionary change of Paramecium bursaria chlorella virus 1 (PBCV-1) during experimental coevolution with its algal host. We used pooled genome sequencing of six independently evolved populations to characterize genomic change over five time points. Across six experimental replicates involving either strong or weak demographic fluctuations, we found single nucleotide polymorphisms (SNPs) at 67 sites. The occurrence of genetic variants was highly repeatable, with just two of the SNPs found in only a single experimental replicate. Three genes A122/123R, A140/145R and A540L showed an excess of variable sites, providing new information about potential targets of selection during Chlorella-Chlorovirus coevolution. Our data indicated that the studied populations were not mutation-limited and experienced strong positive selection. Our investigation highlighted relevant processes governing the evolution of aquatic large dsDNA viruses, which ultimately contributes to a better understanding of the functioning of natural aquatic ecosystems.

Technological advances in DNA sequencing over the last decade now permit the production and curation of large genomic datasets in an increasing number of non‐model species. Additionally, this new data provides the opportunity for combining datasets, resulting in larger studies with a broader taxonomic range. Whilst the development of new sequencing platforms has been beneficial, resulting in a higher throughput of data at a lower per‐base cost, shifts in sequencing technology can also pose challenges for those wishing to combine new sequencing data with data sequenced on older platforms. Here, we outline the types of studies where the use of curated data might be beneficial, and highlight potential biases that might be introduced by combining data from different sequencing platforms. As an example of the challenges associated with combining data across sequencing platforms, we focus on the impact of the shift in Illumina's base calling technology from a four‐channel to a two‐channel system. We caution that when data is combined from these two systems, erroneous guanine base calls that result from the two‐channel chemistry can make their way through a bioinformatic pipeline, eventually leading to inaccurate and potentially misleading conclusions. We also suggest solutions for dealing with such potential artifacts, which make samples sequenced on different sequencing platforms appear more differentiated from one another than they really are. Finally, we stress the importance of archiving tissue samples and the associated sequences for the continued reproducibility and reusability of sequencing data in the face of ever‐changing sequencing platform technology.

Species interactions and coevolution are integral to ecological communities, but we lack empirical information on when and how these interactions generate and purge genetic diversity. Using genomic time series data from host-virus experiments, we found that coevolution occurs through consecutive selective sweeps in both species, with temporal consistency across replicates. Sweeps were accompanied by phenotypic change (resistance or infectivity increases) and expansions in population size. In the host, population expansion enabled rapid generation of genetic diversity in accordance with neutral processes. Viral molecular evolution was, in contrast, confined to few genes, all putative targets of selection. This study demonstrates that molecular evolution during species interactions is shaped by both eco-evolutionary feedback dynamics and interspecific differences in how genetic diversity is generated and maintained.

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.

Recombination, the exchange of DNA between maternal and paternal chromosomes during meiosis, is an essential feature of sexual reproduction in nearly all multicellular organisms. While the role of recombination in the evolution of sex has received theoretical and empirical attention, less is known about how recombination rate itself evolves and what influence this has on evolutionary processes within sexually reproducing organisms. Here, we explore the patterns of, and processes governing recombination in eukaryotes. We summarize patterns of variation, integrating current knowledge with an analysis of linkage map data in 353 organisms. We then discuss proximate and ultimate processes governing recombination rate variation and consider how these influence evolutionary processes. Genome-wide recombination rates (cM/Mb) can vary more than tenfold across eukaryotes, and there is large variation in the distribution of recombination events across closely related taxa, populations and individuals. We discuss how variation in rate and distribution relates to genome architecture, genetic and epigenetic mechanisms, sex, environmental perturbations and variable selective pressures. There has been great progress in determining the molecular mechanisms governing recombination, and with the continued development of new modelling and empirical approaches, there is now also great opportunity to further our understanding of how and why recombination rate varies.
This article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.