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.

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.

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.

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.

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.

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.

Quantifying how constraints limit the diversity of viable routes to adaptation.

Convergent adaptation occurs at the genome scale when independently evolving lineages use the same genes to respond to similar selection pressures. These patterns of genetic repeatability provide insights into the factors that facilitate or constrain the diversity of genetic responses that contribute to adaptive evolution. A first step in studying such factors is to quantify the observed amount of repeatability relative to expectations under a null hypothesis. Here, we formulate a novel index to quantify the constraints driving the observed amount of repeated adaptation in pairwise contrasts based on the hypergeometric distribution, and then generalize this for simultaneous analysis of multiple lineages. This index is explicitly based on the probability of observing a given amount of repeatability by chance under a given null hypothesis and is readily compared among different species and types of trait. We also formulate an index to quantify the effective proportion of genes in the genome that have the potential to contribute to adaptation. As an example of how these indices can be used to draw inferences, we assess the amount of repeatability observed in existing datasets on adaptation to stress in yeast and climate in conifers. This approach provides a method to test a wide range of hypotheses about how different kinds of factors can facilitate or constrain the diversity of genetic responses observed during adaptive evolution.

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.

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.

Purifying selection does not drive signatures of convergent local adaptation of lodgepole pine and interior spruce.

BACKGROUND: Lodgepole pine (Pinus contorta) and interior spruce (Picea glauca, Picea engelmannii, and their hybrids) are distantly related conifer species. Previous studies identified 47 genes containing variants associated with environmental variables in both species, providing evidence of convergent local adaptation. However, if the intensity of purifying selection varies with the environment, clines in nucleotide diversity could evolve through linked (background) selection that would yield allele frequency-environment signatures resembling local adaptation. If similar geographic patterns in the strength of purifying selection occur in these species, this could result in the convergent signatures of local adaptation, especially if the landscape of recombination is conserved. In the present study, we investigated whether spatially/environmentally varying purifying selection could give rise to the convergent signatures of local adaptation that had previously reported. RESULTS: We analyzed 86 lodgepole pine and 50 interior spruce natural populations spanning heterogeneous environments in western Canada where previous analyses had found signatures of convergent local adaptation. We estimated nucleotide diversity and Tajima's D for each gene within each population and calculated the strength of correlations between nucleotide diversity and environmental variables. Overall, these estimates in the genes with previously identified convergent local adaptation signatures had no similar pattern between pine and spruce. Clines in nucleotide diversity along environmental variables were found for interior spruce, but not for lodgepole pine. In spruce, genes with convergent adaption signatures showed a higher strength of correlations than genes without convergent adaption signatures, but there was no such disparity in pine, which suggests the pattern in spruce may have arisen due to a combination of selection and hybridization. CONCLUSIONS: The results rule out purifying/background selection as a driver of convergent local adaption signatures in lodgepole pine and interior spruce.

Mating system impacts the genetic architecture of adaptation to heterogeneous environments.

Self-fertilisation has consequences for variation across the genome as it reduces effective population size, effect recombination rates and pollen flow, with implications for local adaptation. We conducted simulations of divergent stabilising selection on a quantitative trait with drift, pollen flow, mutation, recombination and different outcrossing rates. We quantified trait divergence and the genetic architecture of adaptation. We conducted an FST outlier analysis to identify candidate loci and quantified the impact of mating system on detectability. Selfing promoted trait divergence mainly through reductions in pollen flow. Moreover, trait architecture became more diffuse with selfing. Average effect size of trait loci was lower, while the number of loci, and their clustering distance increased. The genetic architecture of selfers was also more diffuse than outcrossers for equivalent migration rates. However, when deleterious alleles were included, architectures became more concentrated in selfers, likely to be because of reductions in population size caused by mutational meltdown and impacts of background selection on Ne . Our simulations demonstrate that mating system has important impacts on adaptive divergence of traits and the genetic landscape underlying that divergence. Selfing has a significant effect on detectability of regions of the genome important for adaptation because of neutral divergence and diffuse trait architecture.

Rapid and repeated local adaptation to climate in an invasive plant.

Biological invasions provide opportunities to study evolutionary processes occurring over contemporary timescales. To explore the speed and repeatability of adaptation, we examined the divergence of life-history traits to climate, using latitude as a proxy, in the native North American and introduced European and Australian ranges of the annual plant Ambrosia artemisiifolia. We explored niche changes following introductions using climate niche dynamic models. In a common garden, we examined trait divergence by growing seeds collected across three ranges with highly distinct demographic histories. Heterozygosity-fitness associations were used to explore the effect of invasion history on potential success. We accounted for nonadaptive population differentiation using 11 598 single nucleotide polymorphisms. We revealed a centroid shift to warmer, wetter climates in the introduced ranges. We identified repeated latitudinal divergence in life-history traits, with European and Australian populations positioned at either end of the native clines. Our data indicate rapid and repeated adaptation to local climates despite the recent introductions and a bottleneck limiting genetic variation in Australia. Centroid shifts in the introduced ranges suggest adaptation to more productive environments, potentially contributing to trait divergence between the ranges.

Bioinformatically predicted deleterious mutations reveal complementation in the interior spruce hybrid complex.

BACKGROUND: Mutation load is expected to be reduced in hybrids via complementation of deleterious alleles. While local adaptation of hybrids confounds phenotypic tests for reduced mutation load, it may be possible to assess variation in load by analyzing the distribution of putatively deleterious alleles. Here, we use this approach in the interior spruce (Picea glauca x P. engelmannii) hybrid complex, a group likely to suffer from high mutation load and in which hybrids exhibit local adaptation to intermediate conditions. We used PROVEAN to bioinformatically predict whether non-synonymous alleles are deleterious, based on conservation of the position and abnormality of the amino acid change. RESULTS: As expected, we found that predicted deleterious alleles were at lower average allele frequencies than alleles not predicted to be deleterious. We were unable to detect a phenotypic effect on juvenile growth rate of the many rare alleles predicted to be deleterious. Both the proportion of alleles predicted to be deleterious and the proportion of loci homozygous for predicted deleterious alleles were higher in P. engelmannii (Engelmann spruce) than in P. glauca (white spruce), due to higher diversity and frequencies of rare alleles in Engelmann. Relative to parental species, the proportion of alleles predicted to be deleterious was intermediate in hybrids, and the proportion of loci homozygous for predicted deleterious alleles was lowest. CONCLUSION: Given that most deleterious alleles are recessive, this suggests that mutation load is reduced in hybrids due to complementation of deleterious alleles. This effect may enhance the fitness of hybrids.

Expression Divergence Is Correlated with Sequence Evolution but Not Positive Selection in Conifers.

The evolutionary and genomic determinants of sequence evolution in conifers are poorly understood, and previous studies have found only limited evidence for positive selection. Using RNAseq data, we compared gene expression profiles to patterns of divergence and polymorphism in 44 seedlings of lodgepole pine (Pinus contorta) and 39 seedlings of interior spruce (Picea glauca × engelmannii) to elucidate the evolutionary forces that shape their genomes and their plastic responses to abiotic stress. We found that rapidly diverging genes tend to have greater expression divergence, lower expression levels, reduced levels of synonymous site diversity, and longer proteins than slowly diverging genes. Similar patterns were identified for the untranslated regions, but with some exceptions. We found evidence that genes with low expression levels had a larger fraction of nearly neutral sites, suggesting a primary role for negative selection in determining the association between evolutionary rate and expression level. There was limited evidence for differences in the rate of positive selection among genes with divergent versus conserved expression profiles and some evidence supporting relaxed selection in genes diverging in expression between the species. Finally, we identified a small number of genes that showed evidence of site-specific positive selection using divergence data alone. However, estimates of the proportion of sites fixed by positive selection (α) were in the range of other plant species with large effective population sizes suggesting relatively high rates of adaptive divergence among conifers.

Multiple introductions, admixture and bridgehead invasion characterize the introduction history of Ambrosia artemisiifolia in Europe and Australia.

Admixture between differentiated populations is considered to be a powerful mechanism stimulating the invasive success of some introduced species. It is generally facilitated through multiple introductions; however, the importance of admixture prior to introduction has rarely been considered. We assess the likelihood that the invasive Ambrosia artemisiifolia populations of Europe and Australia developed through multiple introductions or were sourced from a historical admixture zone within native North America. To do this, we combine large genomic and sampling data sets analysed with approximate Bayesian computation and random forest scenario evaluation to compare single and multiple invasion scenarios with pre- and postintroduction admixture simultaneously. We show the historical admixture zone within native North America originated before global invasion of this weed and could act as a potential source of introduced populations. We provide evidence supporting the hypothesis that the invasive populations established through multiple introductions from the native range into Europe and subsequent bridgehead invasion into Australia. We discuss the evolutionary mechanisms that could promote invasiveness and evolutionary potential of alien species from bridgehead invasions and admixed source populations.

Comparative genomics in the Asteraceae reveals little evidence for parallel evolutionary change in invasive taxa.

Asteraceae, the largest family of flowering plants, has given rise to many notorious invasive species. Using publicly available transcriptome assemblies from 35 Asteraceae, including six major invasive species, we examined evidence for micro- and macro-evolutionary genomic changes associated with invasion. To detect episodes of positive selection repeated across multiple introductions, we conducted comparisons between native and introduced genotypes from six focal species and identified genes with elevated rates of amino acid change (dN/dS). We then looked for evidence of positive selection at a broader phylogenetic scale across all taxa. As invasive species may experience founder events during colonization and spread, we also looked for evidence of increased genetic load in introduced genotypes. We rarely found evidence for parallel changes in orthologous genes in the intraspecific comparisons, but in some cases we identified changes in members of the same gene family. Using among-species comparisons, we detected positive selection in 0.003-0.69% and 2.4-7.8% of the genes using site and stochastic branch-site models, respectively. These genes had diverse putative functions, including defence response, stress response and herbicide resistance, although there was no clear pattern in the GO terms. There was no indication that introduced genotypes have a higher proportion of deleterious alleles than native genotypes in the six focal species, suggesting multiple introductions and admixture mitigated the impact of drift. Our findings provide little evidence for common genomic responses in invasive taxa of the Asteraceae and hence suggest that multiple evolutionary pathways may lead to adaptation during introduction and spread in these species.

Reproductive isolation during domestication.

It has been hypothesized that reproductive isolation should facilitate evolution under domestication. However, a systematic comparison of reproductive barrier strength between crops and their progenitors has not been conducted to test this hypothesis. Here, we present a systematic survey of reproductive barriers between 32 economically important crop species and their progenitors to better understand the role of reproductive isolation during the domestication process. We took a conservative approach, avoiding those types of reproductive isolation that are poorly known for these taxa (e.g., differences in flowering time). We show that the majority of crops surveyed are isolated from their progenitors by one or more reproductive barriers, despite the fact that the most important reproductive barrier in natural systems, geographical isolation, was absent, at least in the initial stages of domestication for most species. Thus, barriers to reproduction between crops and wild relatives are closely associated with domestication and may facilitate it, thereby raising the question whether reproductive isolation could be viewed as a long-overlooked "domestication trait." Some of the reproductive barriers observed (e.g., polyploidy and uniparental reproduction), however, may have been favored for reasons other than, or in addition to, their effects on gene flow.

Conservation and divergence of gene expression plasticity following c. 140 million years of evolution in lodgepole pine (Pinus contorta) and interior spruce (Picea glauca×Picea engelmannii).

Species respond to environmental stress through a combination of genetic adaptation and phenotypic plasticity, both of which may be important for survival in the face of climatic change. By characterizing the molecular basis of plastic responses and comparing patterns among species, it is possible to identify how such traits evolve. Here, we used de novo transcriptome assembly and RNAseq to explore how patterns of gene expression differ in response to temperature, moisture, and light regime treatments in lodgepole pine (Pinus contorta) and interior spruce (a natural hybrid population of Picea glauca and Picea engelmannii). We found wide evidence for an effect of treatment on expression within each species, with 6413 and 11,658 differentially expressed genes identified in spruce and pine, respectively. Comparing patterns of expression among these species, we found that 74% of all orthologs with differential expression had a pattern that was conserved in both species, despite 140 million yr of evolution. We also found that the specific treatments driving expression patterns differed between genes with conserved versus diverged patterns of expression. We conclude that natural selection has probably played a role in shaping plastic responses to environment in these species.