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.

Metreveli, V., H. Kreft, I. Akobia, Z. Janiashvili, Z. Nonashvili, L. Dzadzamia, Z. Javakhishvili, and A. Gavashelishvili. 2023. Potential Distribution and Suitable Habitat for Chestnut (Castanea sativa). Forests 14: 2076.

Chestnut, Castanea sativa Miller (Fagales: Fagaceae), is an ecologically and economically important tree species of the forest ecosystem in Southern Europe, North-Western Europe, Western Asia, North Africa, and the Caucasus. The distributional range of chestnut in Europe has been highly modified by humans since ancient times. Biotic and abiotic factors have dramatically changed its distribution. Historic anthropogenic range expansion makes it difficult to identify habitat requirements for natural stands of chestnut. In the Caucasus, natural stands of chestnut survived in glacial forest refugia and landscapes that have been difficult for humans to colonize. To identify the species reliable habitat requirements, we estimated the relationship between climatic variables and 620 occurrence locations of natural chestnut stands from the Caucasus and validated the model using GBIF data from outside the Caucasus. We found that our best model is reasonably accurate and the data from the Caucasus characterize chestnut stands throughout the species range well.

Suicmez, B., and M. Avci. 2023. Distribution patterns of Quercus ilex from the last interglacial period to the future by ecological niche modeling. Ecology and Evolution 13.

The plants' geographic distribution is affected by natural or human‐induced climate change. Numerous studies at both the global and regional levels currently focus on the potential changes in plant distribution areas. Ecological niche modeling can help predict the likely distribution of species according to environmental variables under different climate scenarios. In this study, we predicted the potential geographic distributions of Quercus ilex L. (holm oak), a keystone species of the Mediterranean ecosystem, for the Last Interglacial period (LIG: ~130 Ka), the Last Glacial Maximum (LGM: ~22 Ka), mid‐Holocene (MH: ~6 Ka), and future climate scenarios (Representative Concentration Pathway (RCP) 4.5 and 8.5 scenarios) for 2050–2070 obtained from CCSM4 and MIROC‐ESM global climate scenarios respectively. The models were produced with algorithms from the R‐package “biomod2” and assessed by AUC of the receiver operating characteristic plot and true skill statistics. Aside from BIOCLIM (SRE), all model algorithms performed similarly and produced projections that are supported by good evaluation scores, although random forest (RF) slightly outperformed all the others. Additionally, distribution maps generated for the past period were validated through a comparison with pollen data acquired from the Neotoma Pollen Database. The results revealed that southern areas of the Mediterranean Basin, particularly coastal regions, served as long‐term refugia for Q. ilex, which was supported by fossil pollen data. Furthermore, the models suggest long‐term refugia role for Anatolia and we argue that Anatolia may have served as a founding population for the species. Future climate scenarios indicated that Q. ilex distribution varied by region, with some areas experiencing range contractions and others range expands. This study provides significant insights into the vulnerability of the Q. ilex to future climate change in the Mediterranean ecosystem and highlights the crucial role of Anatolia in the species' historical distribution.

Jin, D., Q. Yuan, X. Dai, G. Kozlowski, and Y. Song. 2023. Enhanced precipitation has driven the evolution of subtropical evergreen broad‐leaved forests in eastern China since the early Miocene: Evidence from ring‐cupped oaks. Journal of Systematics and Evolution.

Subtropical evergreen broad‐leaved forest (EBLF) is the predominant vegetation type in eastern China. However, the majority of the region it covers in eastern China was an arid area during the Paleogene. The temporal history and essential factors involved in the evolution of subtropical EBLFs in eastern China remain enigmatic. Here we report on the niche evolution of Quercus section Cyclobalanopsis, which appeared in south China and Japan during the Eocene and became a dominant component of subtropical EBLFs since the Miocene in eastern Asia, using integrative analysis of occurrences, climate data and a dated phylogeny of 35 species in Cyclobalanopsis. Species within clades Cyclobalanoides, Lamellosa, and Helferiana mainly exist in the Himalaya–Hengduan region, adapting to a plateau climate, while species within the other clades mainly live in eastern China under the control of the East Asian monsoon. Reconstructed history showed that significant divergence of climatic tolerance in Cyclobalanopsis began around 19 million years ago (Ma) in the early Miocene. Simultaneously, disparities in precipitation of wettest/warmest quarter and annual precipitation were markedly enhanced in Cyclobalanopsis, especially in the recent eastern clades. During the Miocene, the marked radiation of Cyclobalanopsis and many other dominant taxa of subtropical EBLFs strongly suggest the rapid formation and expansion of subtropical EBLFs in eastern China. Our research highlights that the intensification of the East Asian monsoon and subsequent occupation of new niches by the ancient clades already present in the south may have jointly promoted the formation of subtropical EBLFs in eastern China since the early Miocene.

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.

Tippery, N. P., N. E. Harms, M. F. Purcell, S. H. Hong, P. Häfliger, K. Killoy, A. L. Wolfe, and R. A. Thum. 2023. Assessing the genetic diversity of Nymphoides peltata in the native and adventive range using microsatellite markers. Biological Invasions.

Nymphoides peltata (yellow floating-heart), native to Eurasia, is an invasive plant in the USA, where it grows in relatively isolated but widespread populations. The species is capable of sexual reproduction by seed and asexual reproduction through fragmentation. Although N. peltata is recognized as a noxious weed, little is known about its geographic region of origin or its dispersal mechanisms and relative amount of genetic variation in its adventive range. We conducted a genetic analysis of N. peltata by studying 68 localities across the native range and 47 localities in the adventive range, using microsatellite markers to determine genetic variability within and among populations, and to infer regions in the native range from which invasive plants originated. A large number of sites in the USA were genetically identical to one another, and there were two predominant multilocus allele phenotypes that were distributed in the northern and southern latitudes, respectively. Additional USA sites were similar to one of the predominant genetic profiles, with greater genetic diversity in southern populations. The genetically identical sites are consistent with asexual spread, potentially via anthropogenic mechanisms. Plants across the USA range were observed to produce viable seeds, and some genetic variation could be explained by sexual reproduction. All USA plants were more similar to plants in Europe than they were to plants in Asia, indicating that the plants likely were introduced originally from Europe. The existence of two genetic clusters and their similarity to plants in different parts of Europe constitute evidence for at least two N. peltata introductions into the USA.

Lima, V. P., R. A. Ferreira de Lima, F. Joner, L. D’Orangeville, N. Raes, I. Siddique, and H. ter Steege. 2023. Integrating climate change into agroforestry conservation: A case study on native plant species in the Brazilian Atlantic Forest. Journal of Applied Ecology.

Designing multispecies systems with suitable climatic affinity and identifying species' vulnerability under human‐driven climate change are current challenges to achieve successful adaptation of natural systems. To address this problem, we need to (1) identify groups of species with climatic similarity under climate scenarios and (2) identify areas with high conservation value under predicted climate change.To recognize species with similar climatic niche requirements that can be grouped for mixed cropping in Brazil, we employed ecological niche models (ENMs) and Spearman's ρ for overlap. We also used prioritization algorithms to map areas of high conservation value using two Shared Socioeconomic Pathways (SSP2‐4.5 and SSP5‐8.5) to assess mid‐term (2041–2060) and long‐term (2061–2080) climate change impacts.We identified 15 species groups with finer climatic affinities at different times depicted on hierarchical clustering dendrograms, which can be combined into agroecological agroforestry systems. Furthermore, we highlight the climatically suitable areas for these groups of species, thus providing an outlook of where different species will need to be planted over time to be conserved. In addition, we observed that climate change is predicted to modify the spatial association of these groups under different future climate scenarios, causing a mean negative change in species climatic similarity of 9.5% to 13.7% under SSP2‐4.5 scenario and 9.5% to 10.5% under SSP5‐8.5, for 2041–2060 and 2061–2080, respectively.Synthesis and applications. Our findings provide a framework for agroforestry conservation. The groups of species with finer climatic affinities identified and the climatically suitable areas can be combined into agroecological productive systems, and provide an outlook of where different species may be planted over time. In addition, the conservation priority zones displaying high climate stability for each species individually and all at once can be incorporated into Brazil's conservation plans by policymakers to prioritize specific sites. Lastly, we urge policymakers, conservation organizations and donors to promote interventions involving farmers and local communities, since the species' evaluated have proven to maintain landscapes with productive forest fragments and can be conserved in different Brazilian ecosystems.

Benson, C. W., M. R. Sheltra, P. J. Maughan, E. N. Jellen, M. D. Robbins, B. S. Bushman, E. L. Patterson, et al. 2023. Homoeologous evolution of the allotetraploid genome of Poa annua L. BMC Genomics 24.

Background Poa annua (annual bluegrass) is an allotetraploid turfgrass, an agronomically significant weed, and one of the most widely dispersed plant species on earth. Here, we report the chromosome-scale genome assemblies of P. annua’s diploid progenitors, P. infirma and P. supina, and use multi-omic analyses spanning all three species to better understand P. annua’s evolutionary novelty. Results We find that the diploids diverged from their common ancestor 5.5 – 6.3 million years ago and hybridized to form P. annua  ≤ 50,000 years ago. The diploid genomes are similar in chromosome structure and most notably distinguished by the divergent evolutionary histories of their transposable elements, leading to a 1.7 × difference in genome size. In allotetraploid P. annua, we find biased movement of retrotransposons from the larger (A) subgenome to the smaller (B) subgenome. We show that P. annua’s B subgenome is preferentially accumulating genes and that its genes are more highly expressed. Whole-genome resequencing of several additional P. annua accessions revealed large-scale chromosomal rearrangements characterized by extensive TE-downsizing and evidence to support the Genome Balance Hypothesis. Conclusions The divergent evolutions of the diploid progenitors played a central role in conferring onto P. annua its remarkable phenotypic plasticity. We find that plant genes (guided by selection and drift) and transposable elements (mostly guided by host immunity) each respond to polyploidy in unique ways and that P. annua uses whole-genome duplication to purge highly parasitized heterochromatic sequences. The findings and genomic resources presented here will enable the development of homoeolog-specific markers for accelerated weed science and turfgrass breeding .