Science Enabled by Specimen Data

Kessous, I. M., H. Farooq, W. Testo, M. F. T. Jiménez, B. Neves, A. R. Pinto, F. Salgueiro, et al. 2024. New insights into the classification, diversification, and evolutionary dynamics of bromeliads. Botanical Journal of the Linnean Society. https://doi.org/10.1093/botlinnean/boae074

Abstract The Neotropics have been host to a myriad of geological and climatic events that have shaped the biodiversity present in the region. Bromeliaceae forms one of the most prominent components of the Neotropical flora, being considered the largest group nearly exclusive to the Americas, with almost 4000 species divided into eight subfamilies. Here, we utilize a new time-calibrated molecular phylogeny including 1268 bromeliad taxa and integrate habitat and morphological data to answer the following questions: (i) Are bromeliad subfamilies monophyletic, and did Neogene and Quaternary events in South America coincide with their divergence? (ii) Did naked seeds of berry-fruited species, epiphytic growth, and climatic factors increase bromeliad diversification? Our analysis reconstructed a new topology concerning some recently diverged lineages, with the genus Bromelia emerging as the sister group of a clade including all remaining Bromelioideae lineages + Puyoideae. Miocene events possibly triggered the diversification of bromeliads after a long period of stasis during the Palaeogene. We hypothesize that the morphological shift between Bromelia and Bromelioideae (except Bromelia) is related to the colonization of a new high-elevation environment by Puyoideae in the Andes. Additionally, our results show that naked seeds and the epiphytic growth form positively influence diversification rate, while precipitation, temperature, and elevation have a negative influence. We emphasize the importance of considering a variety of morphological and ecological features to enhance our understanding of bromeliad evolution.

Dantas, V. L., L. C. S. Oliveira, C. R. Marcati, and J. Sonsin‐Oliveira. 2024. Coordination of bark and wood traits underlies forest‐to‐savanna evolutionary transitions. Journal of Biogeography. https://doi.org/10.1111/jbi.14850

Aim To test the hypothesis that adaptive shifts leading to the assembly of tropical savannas involved coordination between bark and wood traits and to understand the underlying mechanisms.LocationTropical South America.TaxonAngiosperms (woody).MethodsWe compiled data on three bark traits (total, inner and outer relative bark thickness), wood density, maximum height, five secondary xylem traits and on species' habitat information (light environment, climate, soil and fire history) for Neotropical savanna, forest and generalist species (biome groups). We tested for pairwise and multivariate associations among traits across species and if biome group and habitat conditions explained species positions along the resulting strategy axes.ResultsTraits covaried along four different axes. The first axis was consistent with a trade‐off between fire (thick barks) and shade tolerance (low bark to diameter ratio, high vessel density) and contributed to differentiate the three biome groups according to the preference for shaded environments. Forest species also differed from savanna and generalist species in a separate axis by being more resource acquisitive. Maximum height and wood density did not strongly trade‐off with bark thickness, although maximum height was negatively covaried with relative outer bark thickness. Preference for shaded conditions was the main driver of variation in the two principal strategy axes, but temperature, fire and soil sand content also explained differences in plant stature between savanna and generalist species.Main ConclusionsAllocation to bark is constrained by trade‐offs with wood, opposing shade‐tolerant and acquisitive forest species to fire‐resistant and conservative savanna species. Rather than a single strategy axis, three axes are necessary to understand the functional differences among savanna, forest and generalist species. Because two of these axes are controlled by light availability, the associated traits tend to covary in space and time, but not across species.

Serra‐Diaz, J. M., J. Borderieux, B. Maitner, C. C. F. Boonman, D. Park, W. Guo, A. Callebaut, et al. 2024. occTest: An integrated approach for quality control of species occurrence data. Global Ecology and Biogeography. https://doi.org/10.1111/geb.13847

Aim Species occurrence data are valuable information that enables one to estimate geographical distributions, characterize niches and their evolution, and guide spatial conservation planning. Rapid increases in species occurrence data stem from increasing digitization and aggregation efforts, and citizen science initiatives. However, persistent quality issues in occurrence data can impact the accuracy of scientific findings, underscoring the importance of filtering erroneous occurrence records in biodiversity analyses.InnovationWe introduce an R package, occTest, that synthesizes a growing open‐source ecosystem of biodiversity cleaning workflows to prepare occurrence data for different modelling applications. It offers a structured set of algorithms to identify potential problems with species occurrence records by employing a hierarchical organization of multiple tests. The workflow has a hierarchical structure organized in testPhases (i.e. cleaning vs. testing) that encompass different testBlocks grouping different testTypes (e.g. environmental outlier detection), which may use different testMethods (e.g. Rosner test, jacknife,etc.). Four different testBlocks characterize potential problems in geographic, environmental, human influence and temporal dimensions. Filtering and plotting functions are incorporated to facilitate the interpretation of tests. We provide examples with different data sources, with default and user‐defined parameters. Compared to other available tools and workflows, occTest offers a comprehensive suite of integrated tests, and allows multiple methods associated with each test to explore consensus among data cleaning methods. It uniquely incorporates both coordinate accuracy analysis and environmental analysis of occurrence records. Furthermore, it provides a hierarchical structure to incorporate future tests yet to be developed.Main conclusionsoccTest will help users understand the quality and quantity of data available before the start of data analysis, while also enabling users to filter data using either predefined rules or custom‐built rules. As a result, occTest can better assess each record's appropriateness for its intended application.

Anest, A., Y. Bouchenak-Khelladi, T. Charles-Dominique, F. Forest, Y. Caraglio, G. P. Hempson, O. Maurin, and K. W. Tomlinson. 2024. Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems. Nature Plants. https://doi.org/10.1038/s41477-024-01649-4

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants. This study explores the evolution of two traits, branching density and spine presence, in the globally distributed plant family Combretaceae. These traits were found to have appeared in a two-step process in response to mammalian herbivory pressure, revealing the importance of large mammals in the evolution of plant architecture diversity.

Putra, A. R., K. A. Hodgins, and A. Fournier‐Level. 2023. Assessing the invasive potential of different source populations of ragweed (Ambrosia artemisiifolia L.) through genomically informed species distribution modelling. Evolutionary Applications. https://doi.org/10.1111/eva.13632

The genetic composition of founding populations is likely to play a key role in determining invasion success. Individual genotypes may differ in habitat preference and environmental tolerance, so their ability to colonize novel environments can be highly variable. Despite the importance of genetic variation on invasion success, its influence on the potential distribution of invaders is rarely investigated. Here, we integrate population genomics and ecological niche models (ENMs) into a single framework to predict the distribution of globally invasive common ragweed (Ambrosia artemisiifolia) in Australia. We identified three genetic clusters for ragweed and used these to construct cluster‐specific ENMs and characterize within‐species niche differentiation. The potential range of ragweed in Australia depended on the genetic composition and continent of origin of the introduced population. Invaders originating from warmer, wetter climates had a broader potential distribution than those from cooler, drier ones. By quantifying this change, we identified source populations most likely to expand the ragweed distribution. As prevention remains the most effective method of invasive species management, our work provides a valuable way of ranking the threat posed by different populations to better inform management decisions.

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. https://doi.org/10.1002/ece3.10747

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.

Thongsangtum, N., J. Huang, S.-F. Li, Y. Thasod, and T. Su. 2023. Calophyllum (Calophyllaceae) from late Oligocene–Early Miocene of Li Basin, northern Thailand and its biogeographic and paleoclimatic implications. Palaeoworld. https://doi.org/10.1016/j.palwor.2023.09.002

Fossils from tropical Asia, which are far from fully investigated, are important for understanding the evolution of plant diversity and the associated surrounding environment there. In this study, we report, as the first record in Thailand, the well-preserved leaf fossils of Calophyllum Linnaeus (Calophyllaceae) from the upper Oligocene–Lower Miocene lacustrine deposits in Li Basin, northern Thailand. The fossils were identified through detailed comparison with leaves of extant and fossil species. These leaf fossils are assigned to Calophyllum based on several key leaf characteristics such as oblanceolate or oblong in shape and parallel secondary veins, nearly perpendicular to the midvein, as well as secondary veins alternate, closely placed, craspedodromous, parallel, dense, and distinct on surface, forming marginal veins. Based on detailed morphological comparison, these fossil leaves are assigned to C. suraikholaensis Awasthi and Prasad, 1990 and Calophyllum sp. The discovery of Calophyllum indicates a montane subtropical to tropical climate in northern Thailand during the Oligocene–Miocene. Together with previous fossil records, these results suggest that this genus probably originated in India during the Paleogene, and spread from India to Indochina during the Neogene, leading to its modern distribution, which currently prefers tropical climates.

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. https://doi.org/10.1093/evolut/qpad140

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.

Vázquez-Rueda, E., A. P. Cuervo-Robayo, and J. Ayala-Berdon. 2023. Forest dependency could be more important than dispersal capacity for habitat connectivity of four species of insectivorous bats inhabiting a highly anthropized region in central Mexico. Mammal Research. https://doi.org/10.1007/s13364-023-00707-0

The maintenance, restoration, and improvement of habitat structure are critical for biodiversity conservation. Under this context, studies assessing habitat connectivity become essential, especially those focused on anthropized regions holding high species richness. We calculated the habitat connectivity of four species of insectivorous bats with different dispersal capacity and habitat preferences in a highly anthropized region in central Mexico, Idionycteris phyllotis and Myotis thysanodes , with a high dispersal capacity and forest-dependency, and Eptesicus fuscus with a low dispersal capacity, and Tadarida brasiliensis with a high dispersal capacity, as the more tolerant bat species to anthropogenic disturbance. We developed niche-based species distribution models to identify suitable habitat patches for each species. We then assessed habitat connectivity and the importance of suitable habitat patches for maintaining connectivity using a graph theory approach. Our results showed that forest dependency was most important than dispersal capacity for connectivity. We also found that the Iztaccíhuatl-Popocatépetl mountain, a National Park comprising 4.2% of natural vegetation in the study area, was the most critical patch for maintaining connectivity for most of the study species. Our study demonstrates the importance of conserving the remnants of natural vegetation for maintaining habitat connectivity within a fragmented landscape and demonstrates the importance of conserving protected areas as well as other remnants of vegetation for the maintenance of habitat connectivity within a fragmented landscape.

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. https://doi.org/10.1111/geb.13737

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.