Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

Temperature and sex shape reproductive barriers in a climate change hotspot.

Climate change is altering species ranges and reproductive interactions in existing ranges, offering species new scope to mate and hybridize. The outcomes will depend on how environmental factors shape reproductive barriers across life stages, yet this is rarely assessed across the environments that species encounter in nature. We assess prezygotic and postzygotic barriers, and their dependence on temperature and parental sex, in species of a reef-building tubeworm (Galeolaria) from a fast-warming biodiversity hotspot in southern Australia. By replicating pure and reciprocal hybrid crosses across 5 temperatures spanning species' thermal ranges, we estimate thermal tolerance curves (defining niches) for crosses and reproductive isolation at each temperature. By also replicating crosses at 3 life stages, we partition the contributions of prezygotic barriers at fertilization, postzygotic barriers at embryogenesis, and postzygotic barriers at larval development to reproductive isolation. We show that barriers are weaker at fertilization and embryogenesis, but stronger and more temperature sensitive at larval development, as species diverge in thermal niche. Asymmetry of barriers between parental sexes, moreover, suggests a complex interplay between niche differentiation and maternal inheritance. Our findings point to a key role for temperature in reproductive isolation, but also challenges for predicting the fate of isolation in future climates.

Assessing the invasive potential of different source populations of ragweed (Ambrosia artemisiifolia L.) through genomically informed species distribution modelling.

The genetic composition of founding populations is likely to play a key role in determining invasion success. Individual genotypes may differ in habitat preference and environmental tolerance, so their ability to colonize novel environments can be highly variable. Despite the importance of genetic variation on invasion success, its influence on the potential distribution of invaders is rarely investigated. Here, we integrate population genomics and ecological niche models (ENMs) into a single framework to predict the distribution of globally invasive common ragweed (Ambrosia artemisiifolia) in Australia. We identified three genetic clusters for ragweed and used these to construct cluster-specific ENMs and characterize within-species niche differentiation. The potential range of ragweed in Australia depended on the genetic composition and continent of origin of the introduced population. Invaders originating from warmer, wetter climates had a broader potential distribution than those from cooler, drier ones. By quantifying this change, we identified source populations most likely to expand the ragweed distribution. As prevention remains the most effective method of invasive species management, our work provides a valuable way of ranking the threat posed by different populations to better inform management decisions.

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.

Temporal collections to study invasion biology.

Biological invasions represent an extraordinary opportunity to study evolution. This is because accidental or deliberate species introductions have taken place for centuries across large geographical scales, frequently prompting rapid evolutionary transitions in invasive populations. Until recently, however, the utility of invasions as evolutionary experiments has been hampered by limited information on the makeup of populations that were part of earlier invasion stages. Now, developments in ancient and historical DNA technologies, as well as the quickening pace of digitization for millions of specimens that are housed in herbaria and museums globally, promise to help overcome this obstacle. In this review, we first introduce the types of temporal data that can be used to study invasions, highlighting the timescale captured by each approach and their respective limitations. We then discuss how ancient and historical specimens as well as data available from prior invasion studies can be used to answer questions on mechanisms of (mal)adaptation, rates of evolution, or community-level changes during invasions. By bridging the gap between contemporary and historical invasive populations, temporal data can help us connect pattern to process in invasion science. These data will become increasingly important if invasions are to achieve their full potential as experiments of evolution in nature.

Haplotype-Resolved, Chromosome-Level Assembly of White Clover (Trifolium repens L., Fabaceae).

White clover (Trifolium repens L.; Fabaceae) is an important forage and cover crop in agricultural pastures around the world and is increasingly used in evolutionary ecology and genetics to understand the genetic basis of adaptation. Historically, improvements in white clover breeding practices and assessments of genetic variation in nature have been hampered by a lack of high-quality genomic resources for this species, owing in part to its high heterozygosity and allotetraploid hybrid origin. Here, we use PacBio HiFi and chromosome conformation capture (Omni-C) technologies to generate a chromosome-level, haplotype-resolved genome assembly for white clover totaling 998 Mbp (scaffold N50 = 59.3 Mbp) and 1 Gbp (scaffold N50 = 58.6 Mbp) for haplotypes 1 and 2, respectively, with each haplotype arranged into 16 chromosomes (8 per subgenome). We additionally provide a functionally annotated haploid mapping assembly (968 Mbp, scaffold N50 = 59.9 Mbp), which drastically improves on the existing reference assembly in both contiguity and assembly accuracy. We annotated 78,174 protein-coding genes, resulting in protein BUSCO completeness scores of 99.6% and 99.3% against the embryophyta_odb10 and fabales_odb10 lineage datasets, respectively.

Large haploblocks underlie rapid adaptation in the invasive weed Ambrosia artemisiifolia.

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. Here, we leverage extensive contemporary and historical collections of Ambrosia artemisiifolia-an aggressively invasive weed and primary cause of pollen-induced hayfever-to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks-indicative of chromosomal inversions-contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolia's global spread across vast climatic gradients.

Climate adaptation and vulnerability of foundation species in a global change hotspot.

Climate change is altering species ranges, and relative abundances within ranges, as populations become differentially adapted and vulnerable to the climates they face. Understanding present species ranges, whether species harbour and exchange adaptive variants, and how variants are distributed across landscapes undergoing rapid change, is therefore crucial to predicting responses to future climates and informing conservation strategies. Such insights are nonetheless lacking for most species of conservation concern. We assess genomic patterns of neutral variation, climate adaptation and climate vulnerability (offsets in predicted distributions of putatively adaptive variants across present and future landscapes) for sister foundation species, the marine tubeworms Galeolaria caespitosa and Galeolaria gemineoa, in a sentinel region for climate change impacts. We find that species are genetically isolated despite uncovering sympatry in their ranges, show parallel and nonparallel signals of thermal adaptation on spatial scales smaller than gene flow across their ranges, and are predicted to face different risks of maladaptation under future temperatures across their ranges. Our findings have implications for understanding local adaptation in the face of gene flow, and generate spatially explicit predictions for climatic disruption of adaptation and species distributions in coastal ecosystems that could guide experimental validation and conservation planning.

Quantitative trait loci mapping reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed.

Biological invasions offer a unique opportunity to investigate evolution over contemporary timescales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species' invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4493 SNPs) and paired this with phenotypic data from an F2 mapping population (n = 336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger, and more tightly linked alleles should underlie rapid local adaptation during invasion, particularly when divergently adapting populations experience high levels of gene flow.

Uncovering the genomic basis of an extraordinary plant invasion.

Invasive species are a key driver of the global biodiversity crisis, but the drivers of invasiveness, including the role of pathogens, remain debated. We investigated the genomic basis of invasiveness in Ambrosia artemisiifolia (common ragweed), introduced to Europe in the late 19th century, by resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In invasive European populations, we found selection signatures in defense genes and lower prevalence of disease-inducing plant pathogens. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from specific microbial enemies likely favored the plant's remarkable success as an invasive species.

Pollen competition in hybridizing Cakile species: How does a latecomer win the race?

PREMISE: Hybridization between cross-compatible species depends on the extent of competition between alternative mates. Even if stigmatic compatibility allows for hybridization, hybridization requires the heterospecific pollen to be competitive. Here, we determined whether conspecific pollen has an advantage in the race to fertilize ovules and the potential handicap to be overcome by heterospecific pollen in invasive Cakile species. METHODS: We used fluorescence microscopy to measure pollen tube growth after conspecific and heterospecific hand-pollination treatments. We then determined siring success in the progeny relative to the timing of heterospecific pollen arrival on the stigma using CAPS markers. RESULTS: In the absence of pollen competition, pollination time and pollen recipient species had a significant effect on the ratio of pollen tube growth. In long-styled C. maritima (outcrosser), pollen tubes grew similarly in both directions. In short-styled C. edentula (selfer), conspecific and heterospecific pollen tubes grew differently. Cakile edentula pollen produced more pollen tubes, revealing the potential for a mating asymmetry whereby C. edentula pollen had an advantage relative to C. maritima. In the presence of pollen competition, siring success was equivalent when pollen deposition was synchronous. However, a moderate 1-h advantage in the timing of conspecific pollination resulted in almost complete assortative mating, while an equivalent delay in conspecific pollination resulted in substantial hybrid formation. CONCLUSIONS: Hybridization can aid the establishment of invasive species through the transfer of adaptive alleles from cross-compatible species, but also lead to extinction through demographic or genetic swamping. Time of pollen arrival on the stigma substantially affected hybridization rate, pointing to the importance of pollination timing in driving introgression and genetic swamping.

Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands.

The nematode Caenorhabditis elegans is among the most widely studied organisms, but relatively little is known about its natural ecology. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. To characterize the niche and genetic diversity of C. elegans on the Hawaiian Islands and to explore how genetic diversity might be influenced by local adaptation, we repeatedly sampled nematodes over a three-year period, measured various environmental parameters at each sampling site, and whole-genome sequenced the C. elegans isolates that we identified. We found that the typical Hawaiian C. elegans niche comprises moderately moist native forests at high elevations (500-1,500 m) where ambient air temperatures are cool (15-20°C). Compared to other Caenorhabditis species found on the Hawaiian Islands (e.g., Caenorhabditis briggsae and Caenorhabditis tropicalis), we found that C. elegans were enriched in native habitats. We measured levels of genetic diversity and differentiation among Hawaiian C. elegans and found evidence of seven genetically distinct groups distributed across the islands. Then, we scanned these genomes for signatures of local adaptation and identified 18 distinct regions that overlap with hyper-divergent regions, which may be maintained by balancing selection and are enriched for genes related to environmental sensing, xenobiotic detoxification, and pathogen resistance. These results provide strong evidence of local adaptation among Hawaiian C. elegans and contribute to our understanding of the forces that shape genetic diversity on the most remote volcanic archipelago in the world.

Genome assembly of an Australian native grass species reveals a recent whole-genome duplication and biased gene retention of genes involved in stress response.

BACKGROUND: The adaptive significance of polyploidy has been extensively debated, and chromosome-level genome assemblies of polyploids can provide insight into this. The Australian grass Bothriochloa decipiens belongs to the BCD clade, a group with a complex history of hybridization and polyploid. This is the first genome assembly and annotation of a species that belongs to this fascinating yet complex group. FINDINGS: Using Illumina short reads, 10X Genomics linked reads, and Hi-C sequencing data, we assembled a highly contiguous genome of B. decipiens, with a total length of 1,218.22 Mb and scaffold N50 of 42.637 Mb. Comparative analysis revealed that the species experienced a relatively recent whole-genome duplication. We clustered the 20 major scaffolds, representing the 20 chromosomes, into the 2 subgenomes of the parental species using unique repeat signatures. We found evidence of biased fractionation and differences in the activity of transposable elements between the subgenomes prior to hybridization. Duplicates were enriched for genes involved in transcription and response to external stimuli, supporting a biased retention of duplicated genes following whole-genome duplication. CONCLUSIONS: Our results support the hypotheses of a biased retention of duplicated genes following polyploidy and point to differences in repeat activity associated with subgenome dominance. B. decipiens is a widespread species with the ability to establish across many soil types, making it a prime candidate for climate change- resilient ecological restoration of Australian grasslands. This reference genome is a valuable resource for future population genomic research on Australian grasses.

Allen Orr and the genetics of adaptation.

Over most of the 20th century, evolutionary biologists predominantly subscribed to a strong form of "micro-mutationism," in which adaptive phenotypic divergence arises from allele frequency changes at many loci, each with a small effect on the phenotype. To be sure, there were well-known examples of large-effect alleles contributing to adaptation, yet such cases were generally regarded as atypical and unrepresentative of evolutionary change in general. In 1998, Allen Orr published a landmark theoretical paper in Evolution, which showed that both small- and large-effect mutations are likely to contribute to "adaptive walks" of a population to an optimum. Coupled with a growing set of empirical examples of large-effect alleles contributing to divergence (e.g., from QTL studies), Orr's paper provided a mathematical formalism that converted many evolutionary biologists from micro-mutationism to a more pluralistic perspective on the genetic basis of evolutionary change. We revisit the theoretical insights emerging from Orr's paper within the historical context leading up to 1998, and track the influence of this paper on the field of evolutionary biology through an examination of its citations over the last two decades and an analysis of the extensive body of theoretical and empirical research that Orr's pioneering paper inspired.

The tip of the iceberg: Genome wide marker analysis reveals hidden hybridization during invasion.

Biological invasions are accelerating, and invasive species can have large economic impacts as well as severe consequences for biodiversity. During invasions, species can interact, potentially resulting in hybridization. Here, we examined two Cakile species, C. edentula and C. maritima (Brassicaceae), that co-occur and may hybridize during range expansion in separate regions of the globe. Cakile edentula invaded each location first, while C. maritima established later, apparently replacing the former. We assessed the evidence for hybridization in western North America and Australia, where both species have been introduced, and identified source populations with 4561 SNPs using Genotype-by-Sequencing. Our results indicate that C. edentula in Australia originated from one region of eastern North America while in western North America it is probably from multiple sources. Cakile maritima in Australia is derived from at least two different parts of Europe while the introduction in western North America is from one. Although morphological evidence of hybridization is generally limited to mixed species populations in Australia and virtually absent elsewhere, our genetic analysis revealed relatively high levels of hybridization in Australia (58% hybrids using Admixture) and supported the presence of hybrids in western North America (16% hybrids using Admixture) and New Zealand. Hybrids might be commonly overlooked in invaders, as identification based solely on morphological traits may represent only the tip of the iceberg. Our study reveals a repeated pattern of invasion, hybridization and apparent replacement of one species by another, which offers an opportunity to investigate the role of hybridization and introgression during invasion.

Genetically Based Trait Differentiation but Lack of Trade-offs between Stress Tolerance and Performance in Introduced Canada Thistle.

Trade-offs between performance and tolerance of abiotic and biotic stress have been proposed to explain both the success of invasive species and frequently observed size differences between native and introduced populations. Canada thistle seeds collected from across the introduced North American and the native European range were grown in benign and stressful conditions (nutrient stress, shading, simulated herbivory, drought, and mowing), to evaluate whether native and introduced individuals differ in performance or stress tolerance. An additional experiment assessed the strength of maternal effects by comparing plants derived from field-collected seeds with those derived from clones grown in the glasshouse. Introduced populations tended to be larger in size, but no trade-off of stress tolerance with performance was detected; introduced populations had either superior performance or equivalent trait values and survivorship in the treatment common gardens. We also detected evidence of parallel latitudinal clines of some traits in both the native and introduced ranges and associations with climate variables in some treatments, consistent with recent climate adaptation within the introduced range. Our results are consistent with rapid adaptation of introduced populations, but, contrary to predictions, the evolution of invasive traits did not come at the cost of reduced stress tolerance.

Parallel flowering time clines in native and introduced ragweed populations are likely due to adaptation.

As introduced species expand their ranges, they often encounter differences in climate which are often correlated with geography. For introduced species, encountering a geographically variable climate sometimes leads to the re-establishment of clines seen in the native range. However, clines can also be caused by neutral processes, and so it is important to gather additional evidence that population differentiation is the result of selection as opposed to nonadaptive processes. Here, we examine phenotypic and genetic differences in ragweed from the native (North America) and introduced (European) ranges. We used a common garden to assess phenotypic differentiation in size and flowering time in ragweed populations. We found significant parallel clines in flowering time in both North America and Europe. Height and branch number had significant clines in North America, and, while not statistically significant, the patterns in Europe were the same. We used SNP data to assess population structure in both ranges and to compare phenotypic differentiation to neutral genetic variation. We failed to detect significant patterns of isolation by distance, geographic patterns in population structure, or correlations between the major axes of SNP variation and phenotypes or latitude of origin. We conclude that the North American clines in size and the parallel clines seen for flowering time are most likely the result of adaptation.

Rapid repeatable phenotypic and genomic adaptation following multiple introductions.

Uncovering the genomic basis of repeated adaption can provide important insights into the constraints and biases that limit the diversity of genetic responses. Demographic processes such as admixture or bottlenecks affect genetic variation underlying traits experiencing selection. The impact of these processes on the genetic basis of adaptation remains, however, largely unexamined empirically. We here test repeatability in phenotypes and genotypes along parallel climatic clines within the native North American and introduced European and Australian Ambrosia artemisiifolia ranges. To do this, we combined multiple lines of evidence from phenotype-environment associations, FST -like outlier tests, genotype-environment associations and genotype-phenotype associations. We used 853 individuals grown in common garden from 84 sampling locations, targeting 19 phenotypes, >83 k SNPs and 22 environmental variables. We found that 17%-26% of loci with adaptive signatures were repeated among ranges, despite alternative demographic histories shaping genetic variation and genetic associations. Our results suggest major adaptive changes can occur on short timescales, with seemingly minimum impacts due to demographic changes linked to introduction. These patterns reveal some predictability of evolutionary change during range expansion, key in a world facing ongoing climate change, and rapid invasive spread.

A lack of genetically compatible mates constrains the spread of an invasive weed.

Introduced populations often experience lag times before invasion, but the mechanisms constraining rapid expansions of introduced populations are unclear. Solidago altissima is a North American native plant with highly invasive Japanese populations and introduced Australian populations that are not invasive despite the climatic and ecological suitability of the region. By contrasting Australian with Japanese populations, we tested the hypothesis that Australian population growth is limited by a lack of long-distance dispersal via seeds owing to a limited number of compatible mates. In the field, Australian populations rarely produced viable seeds. A cross-pollination experiment found that Australian plants are fertile, yet lack compatible mates within Australia. Genetic analysis revealed that Australian individuals descend from a small set of self-incompatible genetic clones, which explains the negligible seed set within Australia. Our results show that low genetic diversity, leading to mate incompatibility, inhibits invasiveness of Australian S.  altissima, and provides compelling evidence for genetic, rather than ecological, factors constraining invasion in Australia.