Science Enabled by Specimen Data

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.

Calvente, A., A. P. Alves da Silva, D. Edler, F. A. Carvalho, M. R. Fantinati, A. Zizka, and A. Antonelli. 2023. Spiny but photogenic: amateur sightings complement herbarium specimens to reveal the bioregions of cacti. American Journal of Botany.

Premise: Cacti are characteristic elements of the Neotropical flora and of major interest for biogeographic, evolutionary, and ecological studies. Here we test global biogeographic boundaries for Neotropical Cactaceae using specimen‐based occurrences coupled with data from visual observations, as a means to tackle the known collection biases in the family.MethodsSpecies richness and record density were assessed for preserved specimens and human observations and a bioregional scheme tailored to Cactaceae was produced using the interactive web application Infomap Bioregions based on data from 261,272 point records cleaned through automated and manual steps.Key ResultsWe find that areas in Mexico and southwestern USA, Eastern Brazil and along the Andean region have the greatest density of records and the highest species richness. Human observations complement information from preserved specimens substantially, especially along the Andes. We propose 24 cacti bioregions, among which the most species‐rich are: northern Mexico/southwestern USA, central Mexico, southern central Mexico, Central America, Mexican Pacific coast, central and southern Andes, northwestern Mexico/extreme southwestern USA, southwestern Bolivia, northeastern Brazil, Mexico/Baja California.ConclusionsThe bioregionalization proposed shows biogeographical boundaries specific to cacti, and can thereby aid further evolutionary, biogeographic, and ecological studies by providing a validated framework for further analyses. This classification builds upon, and is distinctive from, other expert‐derived regionalization schemes for other taxa. Our results showcase how observation data, including citizen‐science records, can complement traditional specimen‐based data for biogeographic research, particularly for taxa with specific specimen collection and preservation challenges and those that are threatened or internationally protected.This article is protected by copyright. All rights reserved.

Freire-Fierro, A., F. Forest, D. S. Devey, J. F. B. Pastore, J. W. Horn, X.-J. Ge, Z. Wang, et al. 2023. Monnina (Polygalaceae), a New World monophyletic genus full of contrasts. Botanical Journal of the Linnean Society.

Endemic to the Neotropics, Monnina is the second largest genus of Polygalaceae, yet little is known about its phylogenetic history, biogeography, and morphological character evolution. To address these knowledge gaps, we conducted Bayesian and maximum likelihood (ML) analyses of nuclear ITS and plastid trnL–F regions to test the monophyly of Monnina s.l. We used this phylogenetic framework to (i) infer divergence time estimates of lineages within the genus and reconstruct their historical biogeography; (ii) reconstruct the evolution of morphological characters of putative ecological and evolutionary importance in Monnina; and (iii) test for correlations between our phylogenetic hypothesis and environmental data. Our results reveal that Monnina is monophyletic with an indehiscent, 1–2-seeded fruit as a synapomorphy for the genus. We identify six clades within Monnina based on our combined phylogenetic results: Clades A, B, and D are primarily distributed in southern and eastern South America, Clades C and E are primarily Central Andean, and Clade F is chiefly distributed in the Northern Andes and Central America. The ancestor of the Monnina stem lineage dispersed from Australia/Africa to South America during the late Eocene to early Oligocene. The divergences of major lineages within the genus began in the early Miocene. We inferred the most recent common ancestor of Monnina to be an herbaceous plant with one-seeded samaroid fruits. The origins of fleshy fruits and shrubby habits are phylogenetically correlated within Monnina, and their concerted convergent evolution may have promoted increased net diversification rates in the two most species-rich subclades of the genus.

Graham, C. D. K., E. J. Forrestel, A. L. Schilmiller, A. T. Zemenick, and M. G. Weber. 2023. Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis. Evolution.

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species’ contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Maurin, O., A. Anest, F. Forest, I. Turner, R. L. Barrett, R. C. Cowan, L. Wang, et al. 2023. Drift in the tropics: Phylogenetics and biogeographical patterns in Combretaceae. Global Ecology and Biogeography.

Aim The aim of this study was to further advance our understanding of the species-rich, and ecologically important angiosperm family Combretaceae to provide new insights into their evolutionary history. We assessed phylogenetic relationships in the family using target capture data and produced a dated phylogenetic tree to assess fruit dispersal modes and patterns of distribution. Location Tropical and subtropical regions. Time Period Cretaceous to present. Major Taxa Studied Family Combretaceae is a member of the rosid clade and comprises 10 genera and more than 500 species, predominantly assigned to genera Combretum and Terminalia, and occurring on all continents and in a wide range of ecosystems. Methods We use a target capture approach and the Angiosperms353 universal probes to reconstruct a robust dated phylogenetic tree for the family. This phylogenetic framework, combined with seed dispersal traits, biome data and biogeographic ranges, allows the reconstruction of the biogeographical history of the group. Results Ancestral range reconstructions suggest a Gondwanan origin (Africa/South America), with several intercontinental dispersals within the family and few transitions between biomes. Relative abundance of fruit dispersal types differed by both continent and biome. However, intercontinental colonizations were only significantly enhanced by water dispersal (drift fruit), and there was no evidence that seed dispersal modes influenced biome shifts. Main Conclusions Our analysis reveals a paradox as drift fruit greatly enhanced dispersal distances at intercontinental scale but did not affect the strong biome conservatism observed.

Kor, L., and M. Diazgranados. 2023. Identifying important plant areas for useful plant species in Colombia. Biological Conservation 284: 110187.

While area-based approaches continue to dominate biodiversity conservation, there is growing recognition of the importance of the human dimensions of biodiversity. We applied the Important Plant Areas (IPA) approach in Colombia to identify key sites for the conservation of plant species with reported human uses. Drawing on the Checklist of Useful Plants of Colombia, we collated 1,045,889 clean occurrence records for 5400 native species from global data repositories and digitized herbaria. Through analysis based on regionalized grid cells, we identified 980 sites meeting IPA thresholds. These are primarily located in forest habitats, with only 19.8 % within existing national natural parks or internationally designated conservation areas. Grid cells were transformed to polygons based on overlapping ecosystems and administrative boundaries to form more meaningful site boundaries. A subsequent two-stage ranking procedure based on conservation value and richness found 46 sites to be of high priority, with 10 selected as top priorities for further investigation and conservation action. These 10 sites support significant populations of 33 threatened useful plant species and represent six of the 13 bioregions of Colombia in just 0.27 % of its land area. To progress from potential to confirmed IPAs, targeted fieldwork is required alongside stakeholder engagement and consultation, crucially involving local resource users. As a megadiverse country ranked second in the world for its botanical richness, effective IPA management would not only contribute to Colombian targets for sustainable development and conservation but would also support global targets to recover biodiversity for both planet and people.

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.

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.

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 .

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.

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.