Science Enabled by Specimen Data

Borges, C. E., R. Von dos Santos Veloso, C. A. da Conceição, D. S. Mendes, N. Y. Ramirez-Cabral, F. Shabani, M. Shafapourtehrany, et al. 2023. Forecasting Brassica napus production under climate change with a mechanistic species distribution model. Scientific Reports 13. https://doi.org/10.1038/s41598-023-38910-3

Brassica napus , a versatile crop with significant socioeconomic importance, serves as a valuable source of nutrition for humans and animals while also being utilized in biodiesel production. The expansion potential of B. napus is profoundly influenced by climatic variations, yet there remains a scarcity of studies investigating the correlation between climatic factors and its distribution. This research employs CLIMEX to identify the current and future ecological niches of B. napus under the RCP 8.5 emission scenario, utilizing the Access 1.0 and CNRM-CM5 models for the time frame of 2040–2059. Additionally, a sensitivity analysis of parameters was conducted to determine the primary climatic factors affecting B. napus distribution and model responsiveness. The simulated outcomes demonstrate a satisfactory alignment with the known current distribution of B. napus , with 98% of occurrence records classified as having medium to high climatic suitability. However, the species displays high sensitivity to thermal parameters, thereby suggesting that temperature increases could trigger shifts in suitable and unsuitable areas for B. napus , impacting regions such as Canada, China, Brazil, and the United States.

Hill, A., M. F. T. Jiménez, N. Chazot, C. Cássia‐Silva, S. Faurby, L. Herrera‐Alsina, and C. D. Bacon. 2023. Apparent effect of range size and fruit colour on palm diversification may be spurious. Journal of Biogeography. https://doi.org/10.1111/jbi.14683

Aim Fruit selection by animal dispersers with different mobility directly impacts plant geographical range size, which, in turn, may impact plant diversification. Here, we examine the interaction between fruit colour, range size and diversification rate in palms by testing two hypotheses: (1) species with fruit colours attractive to birds have larger range sizes due to high dispersal ability and (2) disperser mobility affects whether small or large range size has higher diversification, and intermediate range size is expected to lead to the highest diversification rate regardless of disperser. Location Global. Time Period Contemporary (or present). Major Taxa Studied Palms (Arecaceae). Methods Palm species were grouped based on likely animal disperser group for given fruit colours. Range sizes were estimated by constructing alpha convex hull polygons from distribution data. We examined disperser group, range size or an interaction of both as possible drivers of change in diversification rate over time in a likelihood dynamic model (Several Examined State-dependent Speciation and Extinction [SecSSE]). Models were fitted, rate estimates were retrieved and likelihoods were compared to those of appropriate null models. Results Species with fruit colours associated with mammal dispersal had larger ranges than those with colours associated with bird dispersal. The best fitting SecSSE models indicated that the examined traits were not the primary driver of the heterogeneity in diversification rates in the model. Extinction rate complexity had a marked impact on model performance and on diversification rates. Main Conclusions Two traits related to dispersal mobility, range size and fruit colour, were not identified as the main drivers of diversification in palms. Increased model extinction rate complexity led to better performing models, which indicates that net diversification should be estimated rather than speciation alone. However, increased complexity may lead to incorrect SecSSE model conclusions without careful consideration. Finally, we find palms with more mobile dispersers do not have larger range sizes, meaning other factors are more important determinants of range size.

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. https://doi.org/10.1111/1365-2664.14464

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.

Wilf, P., and R. M. Kooyman. 2023. Do Southeast Asia’s paleo‐Antarctic trees cool the planet? New Phytologist. https://doi.org/10.1111/nph.19067

Many tree genera in the Malesian uplands have Southern Hemisphere origins, often supported by austral fossil records. Weathering the vast bedrock exposures in the everwet Malesian tropics may have consumed sufficient atmospheric CO2 to contribute significantly to global cooling over the past 15 Myr. However, there has been no discussion of how the distinctive regional tree assemblages may have enhanced weathering and contributed to this process. We postulate that Gondwanan‐sourced tree lineages that can dominate higher‐elevation forests played an overlooked role in the Neogene CO2 drawdown that led to the Ice Ages and the current, now‐precarious climate state. Moreover, several historically abundant conifers in Araucariaceae and Podocarpaceae are likely to have made an outsized contribution through soil acidification that increases weathering. If the widespread destruction of Malesian lowland forests continues to spread into the uplands, the losses will threaten unique austral plant assemblages and, if our hypothesis is correct, a carbon sequestration engine that could contribute to cooler planetary conditions far into the future. Immediate effects include the spread of heat islands, significant losses of biomass carbon and forest‐dependent biodiversity, erosion of watershed values, and the destruction of tens of millions of years of evolutionary history.

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. https://doi.org/10.1186/s12864-023-09456-5

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 .

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. https://doi.org/10.1093/botlinnean/boad009

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.

Richard-Bollans, A., C. Aitken, A. Antonelli, C. Bitencourt, D. Goyder, E. Lucas, I. Ondo, et al. 2023. Machine learning enhances prediction of plants as potential sources of antimalarials. Frontiers in Plant Science 14. https://doi.org/10.3389/fpls.2023.1173328

Plants are a rich source of bioactive compounds and a number of plant-derived antiplasmodial compounds have been developed into pharmaceutical drugs for the prevention and treatment of malaria, a major public health challenge. However, identifying plants with antiplasmodial potential can be time-consuming and costly. One approach for selecting plants to investigate is based on ethnobotanical knowledge which, though having provided some major successes, is restricted to a relatively small group of plant species. Machine learning, incorporating ethnobotanical and plant trait data, provides a promising approach to improve the identification of antiplasmodial plants and accelerate the search for new plant-derived antiplasmodial compounds. In this paper we present a novel dataset on antiplasmodial activity for three flowering plant families – Apocynaceae, Loganiaceae and Rubiaceae (together comprising c. 21,100 species) – and demonstrate the ability of machine learning algorithms to predict the antiplasmodial potential of plant species. We evaluate the predictive capability of a variety of algorithms – Support Vector Machines, Logistic Regression, Gradient Boosted Trees and Bayesian Neural Networks – and compare these to two ethnobotanical selection approaches – based on usage as an antimalarial and general usage as a medicine. We evaluate the approaches using the given data and when the given samples are reweighted to correct for sampling biases. In both evaluation settings each of the machine learning models have a higher precision than the ethnobotanical approaches. In the bias-corrected scenario, the Support Vector classifier performs best – attaining a mean precision of 0.67 compared to the best performing ethnobotanical approach with a mean precision of 0.46. We also use the bias correction method and the Support Vector classifier to estimate the potential of plants to provide novel antiplasmodial compounds. We estimate that 7677 species in Apocynaceae, Loganiaceae and Rubiaceae warrant further investigation and that at least 1300 active antiplasmodial species are highly unlikely to be investigated by conventional approaches. While traditional and Indigenous knowledge remains vital to our understanding of people-plant relationships and an invaluable source of information, these results indicate a vast and relatively untapped source in the search for new plant-derived antiplasmodial compounds.

Robin-Champigneul, F., J. Gravendyck, H. Huang, A. Woutersen, D. Pocknall, N. Meijer, G. Dupont-Nivet, et al. 2023. Northward expansion of the southern-temperate podocarp forest during the Early Eocene Climatic Optimum: Palynological evidence from the NE Tibetan Plateau (China). Review of Palaeobotany and Palynology: 104914. https://doi.org/10.1016/j.revpalbo.2023.104914

The debated vegetation response to climate change can be investigated through palynological fossil records from past extreme climate conditions. In this context, the early Eocene (53.3 to 41.2 million years ago (Ma)) is often referred to as a model for a greenhouse Earth. In the Xining Basin, situated on the North-eastern Tibetan Plateau (NETP), this time interval is represented by an extensive and well-dated sedimentary sequence of evaporites and red mudstones. Here we focus on the palynological record of the Early Eocene Climatic Optimum (EECO; 53.3 to 49.1 Ma) and study the fossil gymnosperm pollen composition in these sediments. In addition, we also investigate the nearest living relatives (NLR) or botanical affinity of these genera and the paleobiogeographic implications of their occurrence in the Eocene of the NETP. To reach our objective, we complemented transmitted light microscopy with laser scanning- and electron microscopy techniques, to produce high-resolution images, and illustrate the morphological variation within fossil and extant gymnosperm pollen. Furthermore, a morphometric analysis was carried out to investigate the infra- and intrageneric variation of these and related taxa. To place the data in context we produced paleobiogeographic maps for Phyllocladidites and for other Podocarpaceae, based on data from a global fossil pollen data base, and compare these with modern records from GBIF. We also assessed the climatic envelope of the NLR. Our analyses confirm the presence of Phyllocladidites (NLR Phyllocladus, Podocarpaceae) and Podocarpidites (NLR Podocarpus, Podocarpaceae) in the EECO deposits in the Xining Basin. In addition, a comparative study based on literature suggests that Parcisporites is likely a younger synonym of Phyllocladidites. Our findings further suggest that the Phyllocladidites specimens are derived from a lineage that was much more diverse than previously thought, and which had a much larger biogeographical distribution during the EECO than at present. Based on the climatic envelope of the NLR, we suggest that the paleoclimatic conditions in the Xining Basin were warmer and more humid during the EECO. We conclude that phylloclade-type conifers typical of the southern-temperate podocarp forests, had a northward geographical expansion during the EECO, followed by extirpation.

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. https://doi.org/10.3390/plants12071433

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.

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. https://doi.org/10.1002/tax.12885

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.