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.
Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture ...underlying these adaptations are poorly understood. Here, we genotype 192 great tits (Parus major) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.
Urbanization represents a fierce driver of phenotypic change, yet the molecular mechanisms underlying observed phenotypic patterns are poorly understood. Epigenetic changes are expected to facilitate ...more rapid adaption to changing or novel environments, such as our towns and cities, compared with slow changes in gene sequence. A comparison of liver and blood tissue from great tits Parus major originating from an urban and a forest site demonstrated that urbanization is associated with variation in genome‐wide patterns of DNA methylation. Combining reduced representation bisulphite sequencing with transcriptome data, we revealed habitat differences in DNA methylation patterns that suggest a regulated and coordinated response to the urban environment. In the liver, genomic sites that were differentially methylated between urban‐ and forest‐dwelling birds were over‐represented in regulatory regions of the genome and more likely to occur in expressed genes. DNA methylation levels were also inversely correlated with gene expression at transcription start sites. Furthermore, differentially methylated CpG sites, in liver, were over‐represented in pathways involved in (i) steroid biosynthesis, (ii) superoxide metabolism, (iii) secondary alcohol metabolism, (iv) chylomicron remodelling, (v) cholesterol transport, (vi) reactive oxygen species (ROS) metabolic process and (vii) epithelial cell proliferation. This corresponds with earlier studies identifying diet and exposure to ROS as two of the main drivers of divergence between organisms in urban and nonurban environments. Conversely, in blood, sites that were differentially methylated between urban‐ and forest‐dwelling birds were under‐represented in regulatory regions, more likely to occur in nonexpressed genes and not over‐represented in specific biological pathways. It remains to be determined whether diverging patterns of DNA methylation represent adaptive evolutionary responses and whether the conclusions can be more widely attributed to urbanization.
Animals plastically adjust their physiological and behavioural phenotypes to conform to their social environment--social niche conformance. The degree of sexual competition is a critical part of the ...social environment to which animals adjust their phenotypes, but the underlying genetic mechanisms are poorly understood. We conducted a study to investigate how differences in sperm competition risk affect the gene expression profiles of the testes and two brain areas (posterior pallium and optic tectum) in breeding male zebra finches (Taeniopygia castanotis). In this pre-registered study, we investigated a large sample of 59 individual transcriptomes. We compared two experimental groups: males held in single breeding pairs (low sexual competition) versus those held in two pairs (elevated sexual competition) per breeding cage. Using weighted gene co-expression network analysis (WGCNA), we observed significant effects of the social treatment in all three tissues. However, only the treatment effects found in the pallium were confirmed by an additional randomisation test for statistical robustness. Likewise, the differential gene expression analysis revealed treatment effects only in the posterior pallium (ten genes) and optic tectum (six genes). No treatment effects were found in the testis at the single gene level. Thus, our experiments do not provide strong evidence for transcriptomic adjustment specific to manipulated sperm competition risk. However, we did observe transcriptomic adjustments to the manipulated social environment in the posterior pallium. These effects were polygenic rather than based on few individual genes with strong effects. Our findings are discussed in relation to an accompanying paper using the same animals, which reports behavioural results consistent with the results presented here.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
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.
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Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
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.
Identifying the genetic basis underlying phenotypic divergence and reproductive isolation is a longstanding problem in evolutionary biology. Genetic signals of adaptation and reproductive isolation ...are often confounded by a wide range of factors, such as variation in demographic history or genomic features. Brown trout (
) in the Loch Maree catchment, Scotland, exhibit reproductively isolated divergent life history morphs, including a rare piscivorous (ferox) life history form displaying larger body size, greater longevity and delayed maturation compared to sympatric benthivorous brown trout. Using a dataset of 16,066 SNPs, we analyzed the evolutionary history and genetic architecture underlying this divergence. We found that ferox trout and benthivorous brown trout most likely evolved after recent secondary contact of two distinct glacial lineages, and identified 33 genomic outlier windows across the genome, of which several have most likely formed through selection. We further identified twelve candidate genes and biological pathways related to growth, development and immune response potentially underpinning the observed phenotypic differences. The identification of clear genomic signals divergent between life history phenotypes and potentially linked to reproductive isolation, through size assortative mating, as well as the identification of the underlying demographic history, highlights the power of genomic studies of young species pairs for understanding the factors shaping genetic differentiation.
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.
Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the ...importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into sympatric benthic and pelagic ecotypes across multiple independent lakes. We found that genes differentially spliced between ecotypes were mostly not differentially expressed (<6% overlap) and were involved in different biological processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were involved in metabolism, immunity and growth. Furthermore, alternative splicing and gene expression were mostly controlled by independent cis‐regulatory quantitative trait loci (<3.4% overlap). Cis‐regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7%–10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks (“hub genes”) and were annotated to significantly more gene ontology terms compared to nondifferentially spliced genes, consistent with a higher level of pleiotropy. Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary processes important for local adaptation. This provides novel insights into the importance of contrasting but putatively complementary molecular processes in rapid parallel adaptive evolution.
see also the Perspective by Sarah J. Salisbury, M. Lisette Delgado and Anne C. Dalziel.
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