Effects of genomic and functional diversity on stand-level productivity and performance of non-native Arabidopsis.

Biodiversity can affect the properties of groups of organisms, such as ecosystem function and the persistence of colonizing populations. Genomic data offer a newly available window to diversity, complementary to other measures like taxonomic or phenotypic diversity. We tested whether native genetic diversity in field experimental stands of Arabidopsis thaliana affected their aboveground biomass and fecundity in their colonized range. We constructed some stands of genotypes that we a priori predicted would differ in performance or show overyielding. We found no relationship between genetic diversity and stand total biomass. However, increasing stand genetic diversity increased fecundity in high-resource conditions. Polyculture (multiple genotype) stands consistently yielded less biomass than expected based on the yields of component genotypes in monoculture. This under-yielding was strongest in stands with late-flowering and high biomass genotypes, potentially due to interference competition by these genotypes. Using a new implementation of association mapping, we identified genetic loci whose diversity was associated with stand-level yield, revealing a major flowering time locus associated with under-yielding of polycultures. Our field experiment supports community ecology studies that find a range of diversity-function relationships. Nevertheless, our results suggest diversity in colonizing propagule pools can enhance population fitness. Furthermore, interference competition among genotypes differing in flowering time might limit the advantages of polyculture.

The importance of growing up: juvenile environment influences dispersal of individuals and their neighbours.

Dispersal is a key ecological process that is strongly influenced by both phenotype and environment. Here, we show that juvenile environment influences dispersal not only by shaping individual phenotypes, but also by changing the phenotypes of neighbouring conspecifics, which influence how individuals disperse. We used a model system (Tribolium castaneum, red flour beetles) to test how the past environment of dispersing individuals and their neighbours influences how they disperse in their current environment. We found that individuals dispersed especially far when exposed to a poor environment as adults if their phenotype, or even one-third of their neighbours' phenotypes, were shaped by a poor environment as juveniles. Juvenile environment therefore shapes dispersal both directly, by influencing phenotype, as well as indirectly, by influencing the external social environment. Thus, the juvenile environment of even a minority of individuals in a group can influence the dispersal of the entire group.

Drought regimens predict life history strategies in Heliophila.

Explaining variation in life history strategies is an enduring goal of evolutionary biology and ecology. Early theory predicted that for plants, annual and perennial life histories reflect adaptations to environments that experience alternative drought regimens. Nevertheless, empirical support for this hypothesis from comparative analyses remains lacking. Here, we test classic life history theory in Heliophila L. (Brassicaceae), a diverse genus of flowering plants native to Africa, controlling for phylogeny and integrating 34 yr of satellite-based drought detection with 2192 herbaria occurrence records. We find that the common ancestor of these species was likely to be an annual, and that perenniality and annuality have repeatedly evolved, an estimated seven and five times, respectively. By comparing historical drought regimens, we show that annuals rather than perennial species occur in environments where droughts are significantly more frequent. We also find evidence that annual plants adapt to predictable drought regimens by escaping drought-prone seasons as seeds. These results yield compelling support for longstanding theoretical predictions by revealing the importance of drought frequency and predictability to explain plant life history. More broadly, this work highlights scalable approaches, integrating herbaria records and remote sensing to address outstanding questions in evolutionary ecology.

Homogenization of Populations in the Wildflower, Texas Bluebonnet (Lupinus texensis).

Wildflower seeds are routinely spread along highways and thoroughfares throughout North America as part of federal beautification policy, but the genetic effect of the introduction of these cultivated populations on wild populations of the same species is unknown. Interbreeding may occur between these seeded and wild populations, resulting in several possible outcomes. Here we sample 187 individuals in 12 matched pairs of neighboring wild and seeded populations of the Texas bluebonnet (Lupinus texensis), a species popular in commercially available wildflower seed mixes used by both the Texas Department of Transportation and the public. We use genotyping by sequencing to identify 11741 genome-wide single nucleotide polymorphisms, as well as a smaller number of SNPs from the chloroplast genome, to analyze population structure and genetic diversity within and between the populations. We find a striking lack of population structure both between wild and seeded populations and amongst wild populations. STRUCTURE analyses indicate that all populations are apparently panmictic. This pattern may be explained by extensive swamping of wild populations by seeded germplasm and increased dispersal of semi-domesticated seed across this species' core native range by humans. We discuss the possible negative and positive ramifications of homogenization on the evolutionary future of this popular wildflower species.

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.

What we still don't know about invasion genetics.

Publication of The Genetics of Colonizing Species in 1965 launched the field of invasion genetics and highlighted the value of biological invasions as natural ecological and evolutionary experiments. Here, we review the past 50 years of invasion genetics to assess what we have learned and what we still don't know, focusing on the genetic changes associated with invasive lineages and the evolutionary processes driving these changes. We also suggest potential studies to address still-unanswered questions. We now know, for example, that rapid adaptation of invaders is common and generally not limited by genetic variation. On the other hand, and contrary to prevailing opinion 50 years ago, the balance of evidence indicates that population bottlenecks and genetic drift typically have negative effects on invasion success, despite their potential to increase additive genetic variation and the frequency of peak shifts. Numerous unknowns remain, such as the sources of genetic variation, the role of so-called expansion load and the relative importance of propagule pressure vs. genetic diversity for successful establishment. While many such unknowns can be resolved by genomic studies, other questions may require manipulative experiments in model organisms. Such studies complement classical reciprocal transplant and field-based selection experiments, which are needed to link trait variation with components of fitness and population growth rates. We conclude by discussing the potential for studies of invasion genetics to reveal the limits to evolution and to stimulate the development of practical strategies to either minimize or maximize evolutionary responses to environmental change.

Rapid evolution of an invasive weed.

Trade-offs between performance and the ability to tolerate abiotic and biotic stress have been suggested to explain both the success of invasive species and phenotypic differentiation between native and invasive populations. It is critical to sample broadly across both ranges and to account for latitudinal clines and maternal effects when testing this premise. Wild-collected Centaurea diffusa seeds were grown in benign and stressful conditions (drought, flooding, nutrient stress and simulated herbivory), to evaluate whether native and introduced individuals differ in performance or life history phenotypes. A second experiment used glasshouse-grown seeds to evaluate whether patterns remain comparable when maternal environment is consistent. Many traits differed between ranges, and in all cases but one, invasive individuals grew larger, performed better, or matured later. No trade-off in performance with herbivore defense was evident. Invasive populations may have been released from a trade-off between growth and drought tolerance apparent in the native range. Larger individuals with delayed maturity and greater reproductive potential have evolved in invasive populations, a pattern evident across broad population sampling, and after latitude and maternal environment were considered. Release from abiotic stress tolerance trade-offs may be important for the invasion success of Centaurea diffusa.

Weather and leaf age separately contribute to temporal shifts in phyllosphere community structure and composition.

Microbial communities living on plant leaves can positively or negatively influence plant health and, by extension, can impact whole ecosystems. Most research into the leaf microbiome consists of snapshots, and little is known about how microbial communities change over time. Weather and host physiological characteristics change over time and are often collinear with other time-varying factors, such as substrate availability, making it difficult to separate the factors driving microbial community change. We leveraged repeated measures over the course of an entire year to isolate the relative importance of environmental, host physiological, and substrate age-related factors on the assembly, structure, and composition of leaf-associated fungal communities. We applied both culturing and sequencing approaches to investigate these communities, focusing on a foundational, widely-distributed plant of conservation concern: basin big sagebrush ( Artemisia tridentata subsp. tridentata ). We found that changes in alpha diversity were independently affected by the age of a community and the air temperature. Surprisingly, total fungal abundance and species richness were not positively correlated and responded differently, sometimes oppositely, to weather. With regard to beta diversity, communities were more similar to each other across similar leaf ages, air temperatures, leaf types, and δ 13 C stable isotope ratios. Nine different genera were differentially abundant with air temperature, δ 13 C, leaf type, and leaf age, and a set of 20 genera were continuously present across the year. Our findings highlight the necessity for longer-term, repeated sampling to parse drivers of temporal change in leaf microbial communities. Open Research Statement: All ITS DNA amplicon sequence raw data are deposited in the NCBI Sequence Read Archive (SRA), BioProject number PRJNA1107252, data will be released upon publication. All community data, metadata, taxonomic data, and R code necessary to reproduce these results are deposited in the GitHub repository archived on Zenodo: 10.5281/zenodo.11106439.

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.

Genomics of Compositae weeds: EST libraries, microarrays, and evidence of introgression.

PREMISE OF STUDY: Weeds cause considerable environmental and economic damage. However, genomic characterization of weeds has lagged behind that of model plants and crop species. Here we describe the development of genomic tools and resources for 11 weeds from the Compositae family that will serve as a basis for subsequent population and comparative genomic analyses. Because hybridization has been suggested as a stimulus for the evolution of invasiveness, we also analyze these genomic data for evidence of hybridization. METHODS: We generated 22 expressed sequence tag (EST) libraries for the 11 targeted weeds using Sanger, 454, and Illumina sequencing, compared the coverage and quality of sequence assemblies, and developed NimbleGen microarrays for expression analyses in five taxa. When possible, we also compared the distributions of Ks values between orthologs of congeneric taxa to detect and quantify hybridization and introgression. RESULTS: Gene discovery was enhanced by sequencing from multiple tissues, normalization of cDNA libraries, and especially greater sequencing depth. However, assemblies from short sequence reads sometimes failed to resolve close paralogs. Substantial introgression was detected in Centaurea and Helianthus, but not in Ambrosia and Lactuca. CONCLUSIONS: Transcriptome sequencing using next-generation platforms has greatly reduced the cost of genomic studies of nonmodel organisms, and the ESTs and microarrays reported here will accelerate evolutionary and molecular investigations of Compositae weeds. Our study also shows how ortholog comparisons can be used to approximately estimate the genome-wide extent of introgression and to identify genes that have been exchanged between hybridizing taxa.

Genomics of natural history collections for understanding evolution in the wild.

A long-standing question in biology is how organisms change through time and space in response to their environment. This knowledge is of particular relevance to predicting how organisms might respond to future environmental changes caused by human-induced global change. Usually researchers make inferences about past events based on an understanding of current static genetic patterns, but these are limited in their capacity to inform on underlying past processes. Natural history collections (NHCs) represent a unique and critical source of information to provide temporally deep and spatially broad time-series of samples. By using NHC samples, researchers can directly observe genetic changes over time and space and link those changes with specific ecological/evolutionary events. Until recently, such genetic studies were hindered by the intrinsic challenges of NHC samples (i.e. low yield of highly fragmented DNA). However, recent methodological and technological developments have revolutionized the possibilities in the novel field of NHC genomics. In this Special Feature, we compile a range of studies spanning from methodological aspects to particular case studies which demonstrate the enormous potential of NHC samples for accessing large genomic data sets from the past to advance our knowledge on how populations and species respond to global change at multiple spatial-temporal scales. We also highlight possible limitations, recommendations and a few opportunities for future researchers aiming to study NHC genomics.

Adaptive plasticity and niche expansion in an invasive thistle.

Phenotypic differentiation in size and fecundity between native and invasive populations of a species has been suggested as a causal driver of invasion in plants. Local adaptation to novel environmental conditions through a micro-evolutionary response to natural selection may lead to phenotypic differentiation and fitness advantages in the invaded range. Local adaptation may occur along a stress tolerance trade-off, favoring individuals that, in benign conditions, shift resource allocation from stress tolerance to increased vigor and fecundity and, therefore, invasiveness. Alternately, the typically disturbed invaded range may select for a plastic, generalist strategy, making phenotypic plasticity the main driver of invasion success. To distinguish between these hypotheses, we performed a field common garden and tested for genetically based phenotypic differentiation, resource allocation shifts in response to water limitation, and local adaptation to the environmental gradient which describes the source locations for native and invasive populations of diffuse knapweed (Centaurea diffusa). Plants were grown in an experimental field in France (naturalized range) under water addition and limitation conditions. After accounting for phenotypic variation arising from environmental differences among collection locations, we found evidence of genetic variation between the invasive and native populations for most morphological and life-history traits under study. Invasive C. diffusa populations produced larger, later maturing, and therefore potentially fitter individuals than native populations. Evidence for local adaptation along a resource allocation trade-off for water limitation tolerance is equivocal. However, native populations do show evidence of local adaptation to an environmental gradient, a relationship which is typically not observed in the invaded range. Broader analysis of the climatic niche inhabited by the species in both ranges suggests that the physiological tolerances of C. diffusa may have expanded in the invaded range. This observation could be due to selection for plastic, "general-purpose" genotypes with broad environmental tolerances.

High-throughput genetic identification of functionally important regions of the yeast DEAD-box protein Mss116p.

The Saccharomyces cerevisiae DEAD-box protein Mss116p is a general RNA chaperone that functions in splicing mitochondrial group I and group II introns. Recent X-ray crystal structures of Mss116p in complex with ATP analogs and single-stranded RNA show that the helicase core induces a bend in the bound RNA, as in other DEAD-box proteins, while a C-terminal extension (CTE) induces a second bend, resulting in RNA crimping. Here, we illuminate these structures by using high-throughput genetic selections, unigenic evolution, and analyses of in vivo splicing activity to comprehensively identify functionally important regions and permissible amino acid substitutions throughout Mss116p. The functionally important regions include those containing conserved sequence motifs involved in ATP and RNA binding or interdomain interactions, as well as previously unidentified regions, including surface loops that may function in protein-protein interactions. The genetic selections recapitulate major features of the conserved helicase motifs seen in other DEAD-box proteins but also show surprising variations, including multiple novel variants of motif III (SAT). Patterns of amino acid substitutions indicate that the RNA bend induced by the helicase core depends on ionic and hydrogen-bonding interactions with the bound RNA; identify a subset of critically interacting residues; and indicate that the bend induced by the CTE results primarily from a steric block. Finally, we identified two conserved regions-one the previously noted post II region in the helicase core and the other in the CTE-that may help displace or sequester the opposite RNA strand during RNA unwinding.

Selective sweeps in the homoploid hybrid species Helianthus deserticola: evolution in concert across populations and across origins.

The evolution of different populations within a species in response to selective pressures can potentially happen in three different ways. It can occur in parallel, where similar changes occur independently in each population in response to selection; in concert, where the spread of an adaptive mutation across a species' range results in a single allele fixing in each population; or populations can diverge in response to local selective pressures. We explored these possibilities in populations of the homoploid hybrid species Helianthus deserticola relative to its parental species Helianthus annuus and Helianthus petiolaris using an analysis of variation in 96 expressed sequence tag-based microsatellites. A total of nine loci showed evidence consistent with recent selection at either the species or population level, although two of these genes were discarded because the apparent sweep did not occur relative to the parent from which the locus was derived. Between one and five loci showed a putative sweep across the entire species range with the same microsatellite allele fixed in each population. This pattern is consistent with evolution in concert despite geographical isolation and potential independent origins of the populations. Only one population of H. deserticola showed candidate sweeps that were unique compared to the rest of the species, and this population has also potentially experienced recent admixture with the parental species.

Origin of Macaronesian Sideritis L. (Lamioideae: Lamiaceae) inferred from nuclear and chloroplast sequence datasets.

Sideritis L. (Lamiaceae) comprises approximately 150 species of annuals and perennials distributed chiefly in the Mediterranean region. The majority of the species belong to the continental subgenus Sideritis which is divided into two perennial (Sideritis and Empedoclea) and two annual (Hesiodia and Burgsdorfia) sections. Twenty-three species are woody perennials endemic to the Macaronesian archipelagos of Madeira and the Canary Islands. In an effort to determine the continental origin of the insular group, we constructed independent phylogenies comprising sequence data from both chloroplast and nuclear markers. Sampling included 7 island taxa drawn from the Macaronesian subgenus Marrubiastrum and 25 continental taxa representing all four sections of subgenus Sideritis. Subgenus Marrubiastrum and the two continental perennial sections form well-supported monophyletic groups in both individual and combined analyses. The annual sections are not monophyletic in any analysis; further sampling of annual taxa is needed to resolve these relationships. All analyses identified Sideritis cossoniana, an annual species from Morocco, as the closest continental relative of the Macaronesian group. This contrasts with the hypothesis of earlier workers who suggested that the insular taxa were most closely related to eastern Mediterranean species of the genus. The phylogenies also demonstrate a distinct increase in woodiness among the Macaronesian species relative to their continental congeners, providing further support for the secondary nature of woodiness in island plants.