Science Enabled by Specimen Data

Qin, F., T. Xue, X. Zhang, X. Yang, J. Yu, S. R. Gadagkar, and S. Yu. 2023. Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere. BMC Plant Biology 23.

Background Impatiens sect. Impatiens is distributed across the Northern Hemisphere and has diversified considerably, particularly within the Hengduan Mountains (HDM) in southwest China. Yet, the infra-sectional phylogenetic relationships are not well resolved, largely due to limited taxon sampling and an insufficient number of molecular markers. The evolutionary history of its diversification is also poorly understood. In this study, plastome data and the most complete sampling to date were used to reconstruct a robust phylogenetic framework for this section. The phylogeny was then used to investigate its biogeographical history and diversification patterns, specifically with the aim of understanding the role played by the HDM and past climatic changes in its diversification. Results A stable phylogeny was reconstructed that strongly supported both the monophyly of the section and its division into seven major clades (Clades I-VII). Molecular dating and ancestral area reconstruction suggest that sect. Impatiens originated in the HDM and Southeast China around 11.76 Ma, after which different lineages dispersed to Northwest China, temperate Eurasia, and North America, mainly during the Pliocene and Pleistocene. An intercontinental dispersal event from East Asia to western North America may have occurred via the Bering Land Bridge or Aleutian Islands. The diversification rate was high during its early history, especially with the HDM, but gradually decreased over time both within and outside the HDM. Multiple linear regression analysis showed that the distribution pattern of species richness was strongly associated with elevation range, elevation, and mean annual temperature. Finally, ancestral niche analysis indicated that sect. Impatiens originated in a relatively cool, middle-elevation area. Conclusions We inferred the evolutionary history of sect. Impatiens based on a solid phylogenetic framework. The HDM was the primary source or pump of its diversity in the Northern Hemisphere. Orogeny and climate change may have also shaped its diversification rates, as a steady decrease in the diversification rate coincided with the uplift of the HDM and climate cooling. These findings provide insights into the distribution pattern of sect. Impatiens and other plants in the Northern Hemisphere.

Paquette, H. A., R. T. McMullin, and Y. F. Wiersma. 2023. The importance of taxonomy for determining species distribution: a case study using the disjunct lichen Brodoa oroarctica. Botany.

Species-focused conservation requires a thorough understanding of species’ distributions. Delineating a species’ distribution requires taxonomic knowledge and adequate occurrence data. For plants and fungi, herbaria represent a valuable source of large-scale occurrence data. Advances in digital technology mean that data from many herbarium collections worldwide are now easily accessible. However, species concepts can change over time requiring herbarium records to be re-examined and databases updated, which does not always occur synchronously across all collections. Therefore, non-critical use of these data can promote inaccuracies in understanding species distributions. Taxonomic revisions are common in understudied organisms, such as lichens. Here, we illustrate how changing taxonomy and non-critical acceptance of online data affects our understanding of disjunct distributions, using the lichen Brodoa oroarctica (Krog) Goward as an example. Defining the distribution of the arctic lichen B. oroarctica is confounded by changing taxonomy and uncertainty of herbarium records that pre-date taxonomic revisions. We review the distribution of this species in the literature and in aggregate occurrence databases, and verify herbarium specimens that represent disjunct occurrences in eastern North America to present an updated account of its distribution and frequency in eastern North America. We show that knowledge of changing species taxonomy is essential to depicting accurate species distributions.

Zhang, H., W. Guo, and W. Wang. 2023. The dimensionality reductions of environmental variables have a significant effect on the performance of species distribution models. Ecology and Evolution 13.

How to effectively obtain species‐related low‐dimensional data from massive environmental variables has become an urgent problem for species distribution models (SDMs). In this study, we will explore whether dimensionality reduction on environmental variables can improve the predictive performance of SDMs. We first used two linear (i.e., principal component analysis (PCA) and independent components analysis) and two nonlinear (i.e., kernel principal component analysis (KPCA) and uniform manifold approximation and projection) dimensionality reduction techniques (DRTs) to reduce the dimensionality of high‐dimensional environmental data. Then, we established five SDMs based on the environmental variables of dimensionality reduction for 23 real plant species and nine virtual species, and compared the predictive performance of those with the SDMs based on the selected environmental variables through Pearson's correlation coefficient (PCC). In addition, we studied the effects of DRTs, model complexity, and sample size on the predictive performance of SDMs. The predictive performance of SDMs under DRTs other than KPCA is better than using PCC. And the predictive performance of SDMs using linear DRTs is better than using nonlinear DRTs. In addition, using DRTs to deal with environmental variables has no less impact on the predictive performance of SDMs than model complexity and sample size. When the model complexity is at the complex level, PCA can improve the predictive performance of SDMs the most by 2.55% compared with PCC. At the middle level of sample size, the PCA improved the predictive performance of SDMs by 2.68% compared with the PCC. Our study demonstrates that DRTs have a significant effect on the predictive performance of SDMs. Specifically, linear DRTs, especially PCA, are more effective at improving model predictive performance under relatively complex model complexity or large sample sizes.

Yim, C., E. S. Bellis, V. L. DeLeo, D. Gamba, R. Muscarella, and J. R. Lasky. 2023. Climate biogeography of Arabidopsis thaliana: Linking distribution models and individual variation. Journal of Biogeography.

Aim Patterns of individual variation are key to testing hypotheses about the mechanisms underlying biogeographic patterns. If species distributions are determined by environmental constraints, then populations near range margins may have reduced performance and be adapted to harsher environments. Model organisms are potentially important systems for biogeographical studies, given the available range‐wide natural history collections, and the importance of providing biogeographical context to their genetic and phenotypic diversity.LocationGlobal.TaxonArabidopsis thaliana (‘Arabidopsis’).MethodsWe fit occurrence records to climate data, and then projected the distribution of Arabidopsis under last glacial maximum, current and future climates. We confronted model predictions with individual performance measured on 2194 herbarium specimens, and we asked whether predicted suitability was associated with life history and genomic variation measured on ~900 natural accessions.ResultsThe most important climate variables constraining the Arabidopsis distribution were winter cold in northern and high elevation regions and summer heat in southern regions. Herbarium specimens from regions with lower habitat suitability in both northern and southern regions were smaller, supporting the hypothesis that the distribution of Arabidopsis is constrained by climate‐associated factors. Climate anomalies partly explained interannual variation in herbarium specimen size, but these did not closely correspond to local limiting factors identified in the distribution model. Late‐flowering genotypes were absent from the lowest suitability regions, suggesting slower life histories are only viable closer to the centre of the realized niche. We identified glacial refugia farther north than previously recognized, as well as refugia concordant with previous population genetic findings. Lower latitude populations, known to be genetically distinct, are most threatened by future climate change. The recently colonized range of Arabidopsis was well‐predicted by our native‐range model applied to certain regions but not others, suggesting it has colonized novel climates.Main ConclusionsIntegration of distribution models with performance data from vast natural history collections is a route forward for testing biogeographical hypotheses about species distributions and their relationship with evolutionary fitness across large scales.

Rodríguez-Merino, A. 2023. Identifying and Managing Areas under Threat in the Iberian Peninsula: An Invasion Risk Atlas for Non-Native Aquatic Plant Species as a Potential Tool. Plants 12: 3069.

Predicting the likelihood that non-native species will be introduced into new areas remains one of conservation’s greatest challenges and, consequently, it is necessary to adopt adequate management measures to mitigate the effects of future biological invasions. At present, not much information is available on the areas in which non-native aquatic plant species could establish themselves in the Iberian Peninsula. Species distribution models were used to predict the potential invasion risk of (1) non-native aquatic plant species already established in the peninsula (32 species) and (2) those with the potential to invade the peninsula (40 species). The results revealed that the Iberian Peninsula contains a number of areas capable of hosting non-native aquatic plant species. Areas under anthropogenic pressure are at the greatest risk of invasion, and the variable most related to invasion risk is temperature. The results of this work were used to create the Invasion Risk Atlas for Alien Aquatic Plants in the Iberian Peninsula, a novel online resource that provides information about the potential distribution of non-native aquatic plant species. The atlas and this article are intended to serve as reference tools for the development of public policies, management regimes, and control strategies aimed at the prevention, mitigation, and eradication of non-native aquatic plant species.

Nikkel, E., D. R. Clements, D. Anderson, and J. L. Williams. 2023. Regional habitat suitability for aquatic and terrestrial invasive plant species may expand or contract with climate change. Biological Invasions.

The threat of invasive species to biodiversity and ecosystem structure is exacerbated by the increasingly concerning outlook of predicted climate change and other human influences. Developing preventative management strategies for invasive plant species before they establish is crucial for effective management. To examine how climate change may impact habitat suitability, we modeled the current and future habitat suitability of two terrestrial species, Geranium lucidum and Pilosella officinarum , and two aquatic species, Butomus umbellatus and Pontederia crassipes , that are relatively new invasive plant species regionally, and are currently spreading in the Pacific Northwest (PNW, North America), an area of unique natural areas, vibrant economic activity, and increasing human population. Using North American presence records, downscaled climate variables, and human influence data, we developed an ensemble model of six algorithms to predict the potential habitat suitability under current conditions and projected climate scenarios RCP 4.5, 7.0, and 8.5 for 2050 and 2080. One terrestrial species ( P. officinarum ) showed declining habitat suitability in future climate scenarios (contracted distribution), while the other terrestrial species ( G. lucidum ) showed increased suitability over much of the region (expanded distribution overall). The two aquatic species were predicted to have only moderately increased suitability, suggesting aquatic plant species may be less impacted by climate change. Our research provides a template for regional-scale modelling of invasive species of concern, thus assisting local land managers and practitioners to inform current and future management strategies and to prioritize limited available resources for species with expanding ranges.

Shen, F., S. Xu, Q. Shen, C. Bi, and M. A. Lysak. 2023. The allotetraploid horseradish genome provides insights into subgenome diversification and formation of critical traits. Nature Communications 14.

Polyploidization can provide a wealth of genetic variation for adaptive evolution and speciation, but understanding the mechanisms of subgenome evolution as well as its dynamics and ultimate consequences remains elusive. Here, we report the telomere-to-telomere (T2T) gap-free reference genome of allotetraploid horseradish ( Armoracia rusticana ) sequenced using a comprehensive strategy. The (epi)genomic architecture and 3D chromatin structure of the A and B subgenomes differ significantly, suggesting that both the dynamics of the dominant long terminal repeat retrotransposons and DNA methylation have played critical roles in subgenome diversification. Investigation of the genetic basis of biosynthesis of glucosinolates (GSLs) and horseradish peroxidases reveals both the important role of polyploidization and subgenome differentiation in shaping the key traits. Continuous duplication and divergence of essential genes of GSL biosynthesis (e.g., FMO GS-OX , IGMT , and GH1 gene family) contribute to the broad GSL profile in horseradish. Overall, the T2T assembly of the allotetraploid horseradish genome expands our understanding of polyploid genome evolution and provides a fundamental genetic resource for breeding and genetic improvement of horseradish. Horseradish is a spicy root vegetable and it also produces horseradish peroxidase, an enzyme widely used in biochemistry applications. Here, the authors report its telomere-to-telomere reference genome, reveal subgenome diversification and the effect on the biosynthesis of glucosinolates and horseradish peroxidases.

Cousins-Westerberg, R., N. Dakin, L. Schat, G. Kadereit, and A. M. Humphreys. 2023. Evolution of cold tolerance in the highly stress-tolerant samphires and relatives (Salicornieae: Amaranthaceae). Botanical Journal of the Linnean Society.

Low temperature constitutes one of the main barriers to plant distributions, confining many clades to their ancestrally tropical biome. However, recent evidence suggests that transitions from tropical to temperate biomes may be more frequent than previously thought. Here, we study the evolution of cold and frost tolerance in the globally distributed and highly stress-tolerant Salicornieae (Salicornioideae, Amaranthaceae s.l.). We first generate a phylogenetic tree comprising almost all known species (85-90%), using newly generated (n = 106) and published nuclear-ribosomal and plastid sequences. Next, we use geographical occurrence data to document in which clades and geographical regions cold-tolerant species occur and reconstruct how cold tolerance evolved. Finally, we test for correlated evolution between frost tolerance and the annual life form. We find that frost tolerance has evolved independently in up to four Northern Hemisphere lineages but that annuals are no more likely to evolve frost tolerance than perennials, indicating the presence of different strategies for adapting to cold environments. Our findings add to mounting evidence for multiple independent out-of-the-tropics transitions among close relatives of flowering plants and raise new questions about the ecological and physiological mechanism(s) of adaptation to low temperatures in Salicornieae.

Clemente, K. J. E., and M. S. Thomsen. 2023. High temperature frequently increases facilitation between aquatic foundation species: a global meta‐analysis of interaction experiments between angiosperms, seaweeds, and bivalves. Journal of Ecology.

Many studies have quantified ecological impacts of individual foundation species (FS). However, emerging data suggest that FS often co‐occur, potentially inhibiting or facilitating one another, thereby causing indirect, cascading effects on surrounding communities. Furthermore, global warming is accelerating, but little is known about how interactions between co‐occurring FS vary with temperature.Shallow aquatic sedimentary systems are often dominated by three types of FS: slower‐growing clonal angiosperms, faster‐growing solitary seaweeds, and shell‐forming filter‐ and deposit‐feeding bivalves. Here, we tested the impacts of one FS on another by analyzing manipulative interaction experiments from 148 papers with a global meta‐analysis.We calculated 1,942 (non‐independent) Hedges’ g effect sizes, from 11,652 extracted values over performance responses, such as abundances, growths or survival of FS, and their associated standard deviations and replication levels. Standard aggregation procedures generated 511 independent Hedges’ g that was classified into six types of reciprocal impacts between FS.We found that (i) seaweeds had consistent negative impacts on angiosperms across performance responses, organismal sizes, experimental approaches, and ecosystem types; (ii) angiosperms and bivalves generally had positive impacts on each other (e.g., positive effects of angiosperms on bivalves were consistent across organismal sizes and experimental approaches, but angiosperm effect on bivalve growth and bivalve effect on angiosperm abundance were not significant); (iii) bivalves positively affected seaweeds (particularly on growth responses); (iv) there were generally no net effects of seaweeds on bivalves (except for positive effect on growth) or angiosperms on seaweeds (except for positive effect on ‘other processes’); and (v) bivalve interactions with other FS were typically more positive at higher temperatures, but angiosperm‐seaweed interactions were not moderated by temperature.Synthesis: Despite variations in experimental and spatiotemporal conditions, the stronger positive interactions at higher temperatures suggest that facilitation, particularly involving bivalves, may become more important in a future warmer world. Importantly, addressing research gaps, such as the scarcity of FS interaction experiments from tropical and freshwater systems and for less studied species, as well as testing for density‐dependent effects, could better inform aquatic ecosystem conservation and restoration efforts and broaden our knowledge of FS interactions in the Anthropocene.

Kanmaz, O., T. Şenel, and H. N. Dalfes. 2023. A Modeling Framework to Frame a Biological Invasion: Impatiens glandulifera in North America. Plants 12: 1433.

Biological invasions are a major component of global environmental change with severe ecological and economic consequences. Since eradicating biological invaders is costly and even futile in many cases, predicting the areas under risk to take preventive measures is crucial. Impatiens glandulifera is a very aggressive and prolific invasive species and has been expanding its invasive range all across the Northern hemisphere, primarily in Europe. Although it is currently spread in the east and west of North America (in Canada and USA), studies on its fate under climate change are quite limited compared to the vast literature in Europe. Hybrid models, which integrate multiple modeling approaches, are promising tools for making projections to identify the areas under invasion risk. We developed a hybrid and spatially explicit framework by utilizing MaxEnt, one of the most preferred species distribution modeling (SDM) methods, and we developed an agent-based model (ABM) with the statistical language R. We projected the I. glandulifera invasion in North America, for the 2020–2050 period, under the RCP 4.5 scenario. Our results showed a predominant northward progression of the invasive range alongside an aggressive expansion in both currently invaded areas and interior regions. Our projections will provide valuable insights for risk assessment before the potentially irreversible outcomes emerge, considering the severity of the current state of the invasion in Europe.