Science Enabled by Specimen Data

Silva-Valderrama, I., J.-R. Úrbez-Torres, and T. J. Davies. 2024. From host to host: The taxonomic and geographic expansion of Botryosphaeriaceae. Fungal Biology Reviews 48: 100352.

Fungal pathogens are responsible for 30% of emerging infectious diseases (EIDs) in plants. The risk of a pathogen emerging on a new host is strongly tied to its host breadth; however, the determinants of host range are still poorly understood. Here, we explore the factors that shape host breadth of plant pathogens within Botryosphaeriaceae, a fungal family associated with several devastating diseases in economically important crops. While most host plants are associated with just one or a few fungal species, some hosts appear to be susceptible to infection by multiple fungi. However, the variation in the number of fungal taxa recorded across hosts is not easily explained by heritable plant traits. Nevertheless, we reveal strong evolutionary conservatism in host breadth, with most fungi infecting closely related host plants, but with some notable exceptions that seem to have escaped phylogenetic constraints on host range. Recent anthropogenic movement of plants, including widespread planting of crops, has provided new opportunities for pathogen spillover. We suggest that constraints to pathogen distributions will likely be further disrupted by climate change, and we may see future emergence events in regions where hosts are present but current climate is unfavorable.

Schertler, A., B. Lenzner, S. Dullinger, D. Moser, J. L. Bufford, L. Ghelardini, A. Santini, et al. 2023. Biogeography and global flows of 100 major alien fungal and fungus‐like oomycete pathogens. Journal of Biogeography.

AbstractAimSpreading infectious diseases associated with introduced pathogens can have devastating effects on native biota and human livelihoods. We analyse the global distribution of 100 major alien fungal and oomycete pathogens with substantial socio‐economic and environmental impacts and examine their taxonomy, ecological characteristics, temporal accumulation trajectories, regional hot‐ and coldspots of taxon richness and taxon flows between continents.LocationGlobal.TaxonAlien/cryptogenic fungi and fungus‐like oomycetes, pathogenic to plants or animals.MethodsTo identify over/underrepresented classes and phyla, we performed Chi2 tests of independence. To describe spatial patterns, we calculated the region‐wise richness and identified hot‐ and coldspots, defined as residuals after correcting taxon richness for region area and sampling effort via a quasi‐Poisson regression. We examined the relationship with environmental and socio‐economic drivers with a multiple linear regression and evaluated a potential island effect. Regional first records were pooled over 20‐year periods, and for global flows the links between the native range to the alien regions were mapped.ResultsPeronosporomycetes (Oomycota) were overrepresented among taxa and regional taxon richness was positively correlated with area and sampling effort. While no island effect was found, likely due to host limitations, hotspots were correlated with human modification of terrestrial land, per capita gross domestic product, temperate and tropical forest biomes, and orobiomes. Regional first records have increased steeply in recent decades. While Europe and Northern America were major recipients, about half of the taxa originate from Asia.Main ConclusionsWe highlight the putative importance of anthropogenic drivers, such as land use providing a conducive environment, contact opportunities and susceptible hosts, as well as economic wealth likely increasing colonisation pressure. While most taxa were associated with socio‐economic impacts, possibly partly due to a bias in research focus, about a third show substantial impacts to both socio‐economy and the environment, underscoring the importance of maintaining a wholescale perspective across natural and managed systems.

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.

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.

Huang, T., J. Chen, K. E. Hummer, L. A. Alice, W. Wang, Y. He, S. Yu, et al. 2023. Phylogeny of Rubus (Rosaceae): Integrating molecular and morphological evidence into an infrageneric revision. TAXON.

Rubus (Rosaceae), one of the most complicated angiosperm genera, contains about 863 species, and is notorious for its taxonomic difficulty. The most recent (1910–1914) global taxonomic treatment of the genus was conducted by Focke, who defined 12 subgenera. Phylogenetic results over the past 25 years suggest that Focke's subdivisions of Rubus are not monophyletic, and large‐scale taxonomic revisions are necessary. Our objective was to provide a comprehensive phylogenetic analysis of the genus based on an integrative evidence approach. Morphological characters, obtained from our own investigation of living plants and examination of herbarium specimens are combined with chloroplast genomic data. Our dataset comprised 196 accessions representing 145 Rubus species (including cultivars and hybrids) and all of Focke's subgenera, including 60 endemic Chinese species. Maximum likelihood analyses inferred phylogenetic relationships. Our analyses concur with previous molecular studies, but with modifications. Our data strongly support the reclassification of several subgenera within Rubus. Our molecular analyses agree with others that only R. subg. Anoplobatus forms a monophyletic group. Other subgenera are para‐ or polyphyletic. We suggest a revised subgeneric framework to accommodate monophyletic groups. Character evolution is reconstructed, and diagnostic morphological characters for different clades are identified and discussed. Based on morphological and molecular evidence, we propose a new classification system with 10 subgenera: R. subg. Anoplobatus, R. subg. Batothamnus, R. subg. Chamaerubus, R. subg. Cylactis, R. subg. Dalibarda, R. subg. Idaeobatus, R. subg. Lineati, R. subg. Malachobatus, R. subg. Melanobatus, and R. subg. Rubus. The revised infrageneric nomenclature inferred from our analyses is provided along with synonymy and type citations. Our new taxonomic backbone is the first systematic and complete global revision of Rubus since Focke's treatment. It offers new insights into deep phylogenetic relationships of Rubus and has important theoretical and practical significance for the development and utilization of these important agronomic crops.

Kroonen, G., A. Jakob, A. I. Palmér, P. van Sluis, and A. Wigman. 2022. Indo-European cereal terminology suggests a Northwest Pontic homeland for the core Indo-European languages S. Wichmann [ed.],. PLOS ONE 17: e0275744.

Questions on the timing and the center of the Indo-European language dispersal are central to debates on the formation of the European and Asian linguistic landscapes and are deeply intertwined with questions on the archaeology and population history of these continents. Recent palaeogenomic studies support scenarios in which the core Indo-European languages spread with the expansion of Early Bronze Age Yamnaya herders that originally inhabited the East European steppes. Questions on the Yamnaya and Pre-Yamnaya locations of the language community that ultimately gave rise to the Indo-European language family are heavily dependent on linguistic reconstruction of the subsistence of Proto-Indo-European speakers. A central question, therefore, is how important the role of agriculture was among the speakers of this protolanguage. In this study, we perform a qualitative etymological analysis of all previously postulated Proto-Indo-European terminology related to cereal cultivation and cereal processing. On the basis of the evolution of the subsistence strategies of consecutive stages of the protolanguage, we find that one or perhaps two cereal terms can be reconstructed for the basal Indo-European stage, also known as Indo-Anatolian, but that core Indo-European, here also including Tocharian, acquired a more elaborate set of terms. Thus, we linguistically document an important economic shift from a mostly non-agricultural to a mixed agro-pastoral economy between the basal and core Indo-European speech communities. It follows that the early, eastern Yamnaya of the Don-Volga steppe, with its lack of evidence for agricultural practices, does not offer a perfect archaeological proxy for the core Indo-European language community and that this stage of the language family more likely reflects a mixed subsistence as proposed for western Yamnaya groups around or to the west of the Dnieper River.