Contrasting Patterns of Single Nucleotide Polymorphisms and Structural Variation Across Multiple Invasions.

Genetic divergence is the fundamental process that drives evolution and ultimately speciation. Structural variants (SVs) are large-scale genomic differences within a species or population and can cause functionally important phenotypic differences. Characterizing SVs across invasive species will fill knowledge gaps regarding how patterns of genetic diversity and genetic architecture shape rapid adaptation under new selection regimes. Here, we seek to understand patterns in genetic diversity within the globally invasive European starling, Sturnus vulgaris. Using whole genome sequencing of eight native United Kingdom (UK), eight invasive North America (NA), and 33 invasive Australian (AU) starlings, we examine patterns in genome-wide SNPs and SVs between populations and within Australia. Our findings detail the landscape of standing genetic variation across recently diverged continental populations of this invasive avian. We demonstrate that patterns of genetic diversity estimated from SVs do not necessarily reflect relative patterns from SNP data, either when considering patterns of diversity along the length of the organism's chromosomes (owing to enrichment of SVs in subtelomeric repeat regions), or interpopulation diversity patterns (possibly a result of altered selection regimes or introduction history). Finally, we find that levels of balancing selection within the native range differ across SNP and SV of different classes and outlier classifications. Overall, our results demonstrate that the processes that shape allelic diversity within populations is complex and support the need for further investigation of SVs across a range of taxa to better understand correlations between often well-studied SNP diversity and that of SVs.

Genetic and Phenotypic Consequences of Local Transitions between Sexual and Parthenogenetic Reproduction in the Wild.

AbstractTransitions from sexual to asexual reproduction have occurred in numerous lineages, but it remains unclear why asexual populations rarely persist. In facultatively parthenogenetic animals, all-female populations can arise when males are absent or become extinct, and such populations could help to understand the genetic and phenotypic changes that occur in the initial stages of transitions to asexuality. We investigated a naturally occurring spatial mosaic of mixed-sex and all-female populations of the facultatively parthenogenetic Australian phasmid Megacrania batesii. Analysis of single-nucleotide polymorphisms indicated multiple independent transitions between reproductive modes. All-female populations had much lower heterozygosity and allelic diversity than mixed-sex populations, but we found few consistent differences in fitness-related traits between population types. All-female populations exhibited more frequent and severe deformities in their (flight-incapable) wings but did not show higher rates of appendage loss. All-female populations also harbored more ectoparasites in swamp (but not beach) habitats. Reproductive mode explained little variation in female body size, fecundity, or egg hatch rate. Our results suggest that transitions to parthenogenetic reproduction can lead to dramatic genetic changes with little immediate effect on performance. All-female M. batesii populations appear to consist of high-fitness genotypes that might be able to thrive for many generations in relatively constant and benign environments but could be vulnerable to environmental challenges, such as increased parasite abundance.

Concurrent invasions of European starlings in Australia and North America reveal population-specific differentiation in shared genomic regions.

A species' success during the invasion of new areas hinges on an interplay between the demographic processes common to invasions and the specific ecological context of the novel environment. Evolutionary genetic studies of invasive species can investigate how genetic bottlenecks and ecological conditions shape genetic variation in invasions, and our study pairs two invasive populations that are hypothesized to be from the same source population to compare how each population evolved during and after introduction. Invasive European starlings (Sturnus vulgaris) established populations in both Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European starling populations to determine how demographic processes interact with rapid evolution to generate similar genetic patterns in these recent and replicated invasions. Demographic models indicate that both invasive populations experienced genetic bottlenecks as expected based on invasion history, and we find that specific genomic regions have differentiated even on this short evolutionary timescale. Despite genetic bottlenecks, we suggest that genetic drift alone cannot explain differentiation in at least two of these regions. The demographic boom intrinsic to many invasions as well as potential inversions may have led to high population-specific differentiation, although the patterns of genetic variation are also consistent with the hypothesis that this infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors). We use targeted sampling of replicated invasions to identify and evaluate support for multiple, interacting evolutionary mechanisms that lead to differentiation during the invasion process.

Historical museum samples enable the examination of divergent and parallel evolution during invasion.

During the Anthropocene, Earth has experienced unprecedented habitat loss, native species decline and global climate change. Concurrently, greater globalization is facilitating species movement, increasing the likelihood of alien species establishment and propagation. There is a great need to understand what influences a species' ability to persist or perish within a new or changing environment. Examining genes that may be associated with a species' invasion success or persistence informs invasive species management, assists with native species preservation and sheds light on important evolutionary mechanisms that occur in novel environments. This approach can be aided by coupling spatial and temporal investigations of evolutionary processes. Here we use the common starling, Sturnus vulgaris, to identify parallel and divergent evolutionary change between contemporary native and invasive range samples and their common ancestral population. To do this, we use reduced-representation sequencing of native samples collected recently in northwestern Europe and invasive samples from Australia, together with museum specimens sampled in the UK during the mid-19th century. We found evidence of parallel selection on both continents, possibly resulting from common global selective forces such as exposure to pollutants. We also identified divergent selection in these populations, which might be related to adaptive changes in response to the novel environment encountered in the introduced Australian range. Interestingly, signatures of selection are equally as common within both invasive and native range contemporary samples. Our results demonstrate the value of including historical samples in genetic studies of invasion and highlight the ongoing and occasionally parallel role of adaptation in both native and invasive ranges.

Signatures of selection in a recent invasion reveal adaptive divergence in a highly vagile invasive species.

A detailed understanding of population genetics in invasive populations helps us to identify drivers of successful alien introductions. Here, we investigate putative signals of selection in Australian populations of invasive common starlings, Sturnus vulgaris, and seek to understand how these have been influenced by introduction history. We used reduced representation sequencing to determine population structure, and identify Single Nucleotide Polymorphisms (SNPs) that are putatively under selection. We found that since their introduction into Australia, starling populations have become genetically differentiated despite the potential for high levels of dispersal, and that starlings have responded to selective pressures imposed by a wide range of environmental conditions across their geographic range. Isolation by distance appears to have played a strong role in determining genetic substructure across the starling's Australian range. Analyses of candidate SNPs that are putatively under selection indicated that aridity, precipitation and temperature may be important factors driving adaptive variation across the starling's invasive range in Australia. However, we also noted that the historic introduction regime may leave footprints on sites flagged as being under adaptive selection, and encourage critical interpretation of selection analyses in non-native populations.

The genome of a globally invasive passerine, the common myna, Acridotheres tristis.

In an era of global climate change, biodiversity conservation is receiving increased attention. Conservation efforts are greatly aided by genetic tools and approaches, which seek to understand patterns of genetic diversity and how they impact species health and their ability to persist under future climate regimes. Invasive species offer vital model systems in which to investigate questions regarding adaptive potential, with a particular focus on how changes in genetic diversity and effective population size interact with novel selection regimes. The common myna (Acridotheres tristis) is a globally invasive passerine and is an excellent model species for research both into the persistence of low-diversity populations and the mechanisms of biological invasion. To underpin research on the invasion genetics of this species, we present the genome assembly of the common myna. We describe the genomic landscape of this species, including genome wide allelic diversity, methylation, repeats, and recombination rate, as well as an examination of gene family evolution. Finally, we use demographic analysis to identify that some native regions underwent a dramatic population increase between the two most recent periods of glaciation, and reveal artefactual impacts of genetic bottlenecks on demographic analysis.

Genomic Tools in Biological Invasions: Current State and Future Frontiers.

Human activities are accelerating rates of biological invasions and climate-driven range expansions globally, yet we understand little of how genomic processes facilitate the invasion process. Although most of the literature has focused on underlying phenotypic correlates of invasiveness, advances in genomic technologies are showing a strong link between genomic variation and invasion success. Here, we consider the ability of genomic tools and technologies to (i) inform mechanistic understanding of biological invasions and (ii) solve real-world issues in predicting and managing biological invasions. For both, we examine the current state of the field and discuss how genomics can be leveraged in the future. In addition, we make recommendations pertinent to broader research issues, such as data sovereignty, metadata standards, collaboration, and science communication best practices that will require concerted efforts from the global invasion genomics community.

Genetics and Plasticity Are Responsible for Ecogeographical Patterns in a Recent Invasion.

Patterns of covariation between phenotype and environment are presumed to be reflective of local adaptation, and therefore translate to a meaningful influence on an individual's overall fitness within that specific environment. However, these environmentally driven patterns may be the result of numerous and interacting processes, such as genetic variation, epigenetic variation, or plastic non-heritable variation. Understanding the relative importance of different environmental variables on underlying genetic patterns and resulting phenotypes is fundamental to understanding adaptation. Invasive systems are excellent models for such investigations, given their propensity for rapid evolution. This study uses reduced representation sequencing data paired with phenotypic data to examine whether important phenotypic traits in invasive starlings (Sturnus vulgaris) within Australia appear to be highly heritable (presumably genetic) or appear to vary with environmental gradients despite underlying genetics (presumably non-heritable plasticity). We also sought to determine which environmental variables, if any, play the strongest role shaping genetic and phenotypic patterns. We determined that environmental variables-particularly elevation-play an important role in shaping allelic trends in Australian starlings and may also reinforce neutral genetic patterns resulting from historic introduction regime. We examined a range of phenotypic traits that appear to be heritable (body mass and spleen mass) or negligibly heritable (e.g. beak surface area and wing length) across the starlings' Australian range. Using SNP variants associated with each of these phenotypes, we identify key environmental variables that correlate with genetic patterns, specifically that temperature and precipitation putatively play important roles shaping phenotype in this species. Finally, we determine that overall phenotypic variation is correlated with underlying genetic variation, and that these interact positively with the level of vegetation variation within a region, suggesting that ground cover plays an important role in shaping selection and plasticity of phenotypic traits within the starlings of Australia.

Evolutionary genomics: Insights from the invasive European starlings.

Two fundamental questions for evolutionary studies are the speed at which evolution occurs, and the way that this evolution may present itself within an organism's genome. Evolutionary studies on invasive populations are poised to tackle some of these pressing questions, including understanding the mechanisms behind rapid adaptation, and how it facilitates population persistence within a novel environment. Investigation of these questions are assisted through recent developments in experimental, sequencing, and analytical protocols; in particular, the growing accessibility of next generation sequencing has enabled a broader range of taxa to be characterised. In this perspective, we discuss recent genetic findings within the invasive European starlings in Australia, and outline some critical next steps within this research system. Further, we use discoveries within this study system to guide discussion of pressing future research directions more generally within the fields of population and evolutionary genetics, including the use of historic specimens, phenotypic data, non-SNP genetic variants (e.g., structural variants), and pan-genomes. In particular, we emphasise the need for exploratory genomics studies across a range of invasive taxa so we can begin understanding broad mechanisms that underpin rapid adaptation in these systems. Understanding how genetic diversity arises and is maintained in a population, and how this contributes to adaptability, requires a deep understanding of how evolution functions at the molecular level, and is of fundamental importance for the future studies and preservation of biodiversity across the globe.

Transcript- and annotation-guided genome assembly of the European starling.

The European starling, Sturnus vulgaris, is an ecologically significant, globally invasive avian species that is also suffering from a major decline in its native range. Here, we present the genome assembly and long-read transcriptome of an Australian-sourced European starling (S. vulgaris vAU), and a second, North American, short-read genome assembly (S. vulgaris vNA), as complementary reference genomes for population genetic and evolutionary characterization. S. vulgaris vAU combined 10× genomics linked-reads, low-coverage Nanopore sequencing, and PacBio Iso-Seq full-length transcript scaffolding to generate a 1050 Mb assembly on 6222 scaffolds (7.6 Mb scaffold N50, 94.6% busco completeness). Further scaffolding against the high-quality zebra finch (Taeniopygia guttata) genome assigned 98.6% of the assembly to 32 putative nuclear chromosome scaffolds. Species-specific transcript mapping and gene annotation revealed good gene-level assembly and high functional completeness. Using S. vulgaris vAU, we demonstrate how the multifunctional use of PacBio Iso-Seq transcript data and complementary homology-based annotation of sequential assembly steps (assessed using a new tool, saaga) can be used to assess, inform, and validate assembly workflow decisions. We also highlight some counterintuitive behaviour in traditional busco metrics, and present buscomp, a complementary tool for assembly comparison designed to be robust to differences in assembly size and base-calling quality. This work expands our knowledge of avian genomes and the available toolkit for assessing and improving genome quality. The new genomic resources presented will facilitate further global genomic and transcriptomic analysis on this ecologically important species.