Science Enabled by Specimen Data

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.

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.

Geier, C., J. M. Bouchal, S. Ulrich, D. Uhl, T. Wappler, S. Wedmann, R. Zetter, et al. 2023. Potential pollinators and paleoecological aspects of Eocene Ludwigia (Onagraceae) from Eckfeld, Germany. Palaeoworld.

Paleogene flower-insect interactions and paleo-pollination processes are, in general, poorly understood and fossil evidence for such floral and faunal interactions are rarely reported. To shed light on angiosperm flower-insect interactions, we investigated several hundred fossil flowers and insects from the middle Eocene Fossil Lagerstätte of Eckfeld, Germany. During our work, we discovered a unique fossil Ludwigia flower (bud) with in situ pollen. The ecological preferences (climate, biome, habitat, etc.) of extant Ludwigia and the paleoecological configurations of the fossil plant assemblage support the taxonomic affiliation of the flower bud and an Eocene presence of Ludwigia in the vicinity of the former Lake Eckfeld. Today’s Ludwigia are mostly pollinated by Hymenoptera (bees). Therefore, we screened all currently known hymenopteran fossils from Eckfeld but found no Ludwigia pollen adhering to any of the specimens. On the contrary, we discovered Ludwigia pollen adhering to two different groups of Coleoptera (beetles). Our study suggests that during the Eocene of Europe, Ludwigia flowers were visited and probably pollinated by beetles and over time there was a shift in primary flower visitors/pollinators, from beetles to bees, sometime during the late Paleogene to Neogene.

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.

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.

Pang, S. E. H., J. W. F. Slik, D. Zurell, and E. L. Webb. 2023. The clustering of spatially associated species unravels patterns in tropical tree species distributions. Ecosphere 14.

Complex distribution data can be summarized by grouping species with similar or overlapping distributions to unravel spatial patterns and separate trends (e.g., of habitat loss) among spatially unique groups. However, such classifications are often heuristic, lacking the transparency, objectivity, and data‐driven rigor of quantitative methods, which limits their interpretability and utility. Here, we develop and illustrate the clustering of spatially associated species, a methodological framework aimed at statistically classifying species using explicit measures of interspecific spatial association. We investigate several association indices and clustering algorithms and show how these methodological choices drive substantial variations in clustering outcomes and performance. To facilitate robust decision‐making, we provide guidance on choosing methods appropriate to one's study objective(s). As a case study, we apply our framework to modeled tree distributions in Borneo and subsequently evaluate the impact of land‐cover change on separate species groupings. Based on the modeled distribution of 390 tree species prior to anthropogenic land‐cover changes, we identified 11 distinct clusters that unraveled ecologically meaningful patterns in Bornean tree distributions. These clusters then enabled us to quantify trends of habitat loss tied to each of those specific clusters, allowing us to discern particularly vulnerable species clusters and their distributions. This study demonstrates the advantages of adopting quantitatively derived clusters of spatially associated species and elucidates the potential of resultant clusters as a spatially explicit framework for investigating distribution‐related questions in ecology, biogeography, and conservation. By adopting our methodological framework and publicly available codes, practitioners can leverage the ever‐growing abundance of distribution data to better understand complex spatial patterns among species distributions and the disparate effects of global changes on biodiversity.

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 .

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.

Franzese, J., and R. R. Ripa. 2023. Common juniper, an overlooked conifer with high invasion potential in protected areas of Patagonia. Scientific Reports 13.

The benefits of early detection of biological invasions are widely recognized, especially for protected areas (PAs). However, research on incipient invasive plant species is scarce compared to species with a recognized history of invasion. Here, we characterized the invasion status of the non-native conifer Juniperus communis in PAs and interface areas of Andean Patagonia, Argentina. We mapped its distribution and described both the invasion and the environments this species inhabits through field studies, a literature review, and a citizen science initiative. We also modeled the species’ potential distribution by comparing the climatic characteristics of its native range with those of the introduced ranges studied. The results show that J. communis is now widely distributed in the region, occurring naturally in diverse habitats, and frequently within and close to PAs. This species can be considered an incipient invader with a high potential for expansion in its regional distribution range, largely due to its high reproductive potential and the high habitat suitability of this environment. Early detection of a plant invasion affords a valuable opportunity to inform citizens of the potential risks to high conservation value ecosystems before the invader is perceived as a natural component of the landscape.

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.