Search

Understanding the extent to which ecological divergence is repeatable is essential for predicting responses of biodiversity to environmental change. Here we test the predictability of evolution, from genotype to phenotype, by studying parallel evolution in a salmonid fish, Arctic charr (Salvelinus alpinus), across eleven replicate sympatric ecotype pairs (benthivorous-planktivorous and planktivorous-piscivorous) and two evolutionary lineages. We found considerable variability in eco-morphological divergence, with several traits related to foraging (eye diameter, pectoral fin length) being highly parallel even across lineages. This suggests repeated and predictable adaptation to environment. Consistent with ancestral genetic variation, hundreds of loci were associated with ecotype divergence within lineages of which eight were shared across lineages. This shared genetic variation was maintained despite variation in evolutionary histories, ranging from postglacial divergence in sympatry (ca. 10-15kya) to pre-glacial divergence (ca. 20-40kya) with postglacial secondary contact. Transcriptome-wide gene expression (44,102 genes) was highly parallel across replicates, involved biological processes characteristic of ecotype morphology and physiology, and revealed parallelism at the level of regulatory networks. This expression divergence was not only plastic but in part genetically controlled by parallel cis-eQTL. Lastly, we found that the magnitude of phenotypic divergence was largely correlated with the genetic differentiation and gene expression divergence. In contrast, the direction of phenotypic change was mostly determined by the interplay of adaptive genetic variation, gene expression, and ecosystem size. Ecosystem size further explained variation in putatively adaptive, ecotype-associated genomic patterns within and across lineages, highlighting the role of environmental variation and stochasticity in parallel evolution. Together, our findings demonstrate the parallel evolution of eco-morphology and gene expression within and across evolutionary lineages, which is controlled by the interplay of environmental stochasticity and evolutionary contingencies, largely overcoming variable evolutionary histories and genomic backgrounds., Competing Interests: The authors have declared that no competing interests exist.

The rapid expansion of three-spined stickleback (Gasterosteus aculeatus Linnaeus, 1758 (Perciformes, Gasterosteida)) in the pelagic zone of Lake Constance, Central Europe, since 2012 contributed to stark ecosystem-wide effects, such as food-web shifts and declines in native biodiversity, including commercially important fish species. Yet, the origin of this invasive pelagic population remains unclear. Using RAD-sequencing of Lake Constance sticklebacks, we show that the pelagic Lake Constance population likely arose recently within the lake, potentially from the littoral population. We did not detect any substantial genome-wide genetic differentiation between individuals from different habitats, supporting a recent origin of the pelagic population and/or ongoing gene flow. This is further supported by minimal differences in meristic and morphometric traits. However, we also identified multiple outlier loci between littoral and pelagic individuals across the genome, potentially suggesting early signs of adaptation despite high connectivity. In this study, we provide an important example of rapid within-lake ecological diversification of an invasive species from standing genetic variation. Ultimately, our findings will have major implications for the management of invasive pelagic stickleback, as they indicate that the stickleback population has to be managed as a whole and that management efforts cannot only focus on the hyper-abundant pelagic population. [ABSTRACT FROM AUTHOR]

Regulation of gene expression plays a central role in adaptive divergence and evolution. Although the role of gene regulation in microevolutionary processes is gaining wide acceptance, most studies have only investigated the evolution of transcript levels, ignoring the potentially significant role of transcript structures. We argue that variation in alternative splicing plays an important and widely unexplored role in adaptation (e.g., by increasing transcriptome and/or proteome diversity, or buffering potentially deleterious genetic variation). New studies increasingly highlight the potential for independent evolution in alternative splicing and transcript level, providing alternative paths for selection to act upon. We propose that alternative splicing and transcript levels can provide contrasting, nonredundant mechanisms of equal importance for adaptive diversification of gene function and regulation. Transcriptional and post-transcriptional regulation of gene expression plays an integral role in development, physiology, and adaptation. Recent studies indicate that variation in transcription and alternative splicing have distinct genetic bases, allowing transcript levels and alternative splicing to evolve independently. Rapid technological development has opened (nearly) all organisms to the investigation of the role of alternative splicing in adaptation. Alternative splicing potentially provides a mechanism for reducing constraints on highly pleiotropic genes. Transcript levels and transcript splicing may play complementary or contrasting roles in adaptive evolution. [ABSTRACT FROM AUTHOR]

Low‐coverage whole genome sequencing (lcWGS) has emerged as a powerful and cost‐effective approach for population genomic studies in both model and nonmodel species. However, with read depths too low to confidently call individual genotypes, lcWGS requires specialized analysis tools that explicitly account for genotype uncertainty. A growing number of such tools have become available, but it can be difficult to get an overview of what types of analyses can be performed reliably with lcWGS data, and how the distribution of sequencing effort between the number of samples analysed and per‐sample sequencing depths affects inference accuracy. In this introductory guide to lcWGS, we first illustrate how the per‐sample cost for lcWGS is now comparable to RAD‐seq and Pool‐seq in many systems. We then provide an overview of software packages that explicitly account for genotype uncertainty in different types of population genomic inference. Next, we use both simulated and empirical data to assess the accuracy of allele frequency, genetic diversity, and linkage disequilibrium estimation, detection of population structure, and selection scans under different sequencing strategies. Our results show that spreading a given amount of sequencing effort across more samples with lower depth per sample consistently improves the accuracy of most types of inference, with a few notable exceptions. Finally, we assess the potential for using imputation to bolster inference from lcWGS data in nonmodel species, and discuss current limitations and future perspectives for lcWGS‐based population genomics research. With this overview, we hope to make lcWGS more approachable and stimulate its broader adoption. [ABSTRACT FROM AUTHOR]

The levels and distribution of standing genetic variation in a genome can provide a wealth of insights about the adaptive potential, demographic history, and genome structure of a population or species. As structural variants are increasingly associated with traits important for adaptation and speciation, investigating both sequence and structural variation is essential for wholly tapping this potential. Using a combination of shotgun sequencing, 10x Genomics linked reads and proximity-ligation data (Chicago and Hi-C), we produced and annotated a chromosome-level genome assembly for the Atlantic silverside (Menidia menidia)—an established ecological model for studying the phenotypic effects of natural and artificial selection—and examined patterns of genomic variation across two individuals sampled from different populations with divergent local adaptations. Levels of diversity varied substantially across each chromosome, consistently being highly elevated near the ends (presumably near telomeric regions) and dipping to near zero around putative centromeres. Overall, our estimate of the genome-wide average heterozygosity in the Atlantic silverside is among the highest reported for a fish, or any vertebrate (1.32–1.76% depending on inference method and sample). Furthermore, we also found extreme levels of structural variation, affecting ∼23% of the total genome sequence, including multiple large inversions (> 1 Mb and up to 12.6 Mb) associated with previously identified haploblocks showing strong differentiation between locally adapted populations. These extreme levels of standing genetic variation are likely associated with large effective population sizes and may help explain the remarkable adaptive divergence among populations of the Atlantic silverside. [ABSTRACT FROM AUTHOR]