Science Enabled by Specimen Data

Ramírez-Barahona, S. 2024. Incorporating fossils into the joint inference of phylogeny and biogeography of the tree fern order Cyatheales R. Warnock, and M. Zelditch [eds.],. Evolution.

Present-day geographic and phylogenetic patterns often reflect the geological and climatic history of the planet. Neontological distribution data are often sufficient to unravel a lineage’s biogeographic history, yet ancestral range inferences can be at odds with fossil evidence. Here, I use the fossilized birth–death process and the dispersal–extinction cladogenesis model to jointly infer the dated phylogeny and range evolution of the tree fern order Cyatheales. I use data for 101 fossil and 442 extant tree ferns to reconstruct the biogeographic history of the group over the last 220 million years. Fossil-aware reconstructions evince a prolonged occupancy of Laurasia over the Triassic–Cretaceous by Cyathealean tree ferns, which is evident in the fossil record but hidden from analyses relying on neontological data alone. Nonetheless, fossil-aware reconstructions are affected by uncertainty in fossils’ phylogenetic placement, taphonomic biases, and specimen sampling and are sensitive to interpretation of paleodistributions and how these are scored. The present results highlight the need and challenges of incorporating fossils into joint inferences of phylogeny and biogeography to improve the reliability of ancestral geographic range estimation.

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.

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.

Prochazka, L. S., S. Alcantara, J. G. Rando, T. Vasconcelos, R. C. Pizzardo, and A. Nogueira. 2024. Resource availability and disturbance frequency shape evolution of plant life forms in Neotropical habitats. New Phytologist.

Organisms use diverse strategies to thrive in varying habitats. While life history theory partly explains these relationships, the combined impact of resource availability and disturbance frequency on life form strategy evolution has received limited attention.We use Chamaecrista species, a legume plant lineage with a high diversity of plant life forms in the Neotropics, and employ ecological niche modeling and comparative phylogenetic methods to examine the correlated evolution of plant life forms and environmental niches.Chamaephytes and phanerophytes have optima in environments characterized by moderate water and nutrient availability coupled with infrequent fire disturbances. By contrast, annual plants thrive in environments with scarce water and nutrients, alongside frequent fire disturbances. Similarly, geophyte species also show increased resistance to frequent fire disturbances, although they thrive in resource‐rich environments.Our findings shed light on the evolution of plant strategies along environmental gradients, highlighting that annuals and geophytes respond differently to high incidences of fire disturbances, with one enduring it as seeds in a resource‐limited habitat and the other relying on reserves and root resprouting systems in resource‐abundant habitats. Furthermore, it deepens our understanding of how organisms evolve associated with their habitats, emphasizing a constraint posed by low‐resource and high‐disturbance environments.

Liendo, D., J. A. Campos, and A. Gandarillas. 2023. Cortaderia selloana, an example of aggressive invaders that affect human health, yet to be included in binding international invasive catalogues. NeoBiota 89: 229–237.

Invasive plant species can suppress local biodiversity, affect soil properties and modify the landscape. However, an additional concern of plant invasions that has been more disregarded is their impact on environmental human health. Here, we discuss the case of Cortaderia selloana (Schult. & Schult.f.) Asch. & Graebn, as an example of a worldwide invasive species with a strong environmental impact. We summarise the main facts regarding the C. selloana invasion, the recent clinical evidence of its impact on human health and the great potential expansion of the species in the context of climate change. C. selloana constitutes a clear example to boost demands from policy makers for urgent and efficient measures to control or eradicate invasive species, also in ruderal areas. This aggressive invader is still out of relevant binding international invasive species catalogues, including the European List of Invasive Alien Species of Union concern (Union list), and is still subjected to extensive trading in some European countries. Therefore, including C. selloana in the Union list becomes mandatory to impose full restrictions on keeping, importing, selling, breeding and cultivating the species.

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.

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.

García-Navarrete, P. G., L. A. Sánchez-González, and J. J. Morrone. 2023. Biogeographical affinities of the biota of the Tres Marías Islands, Mexico. Biological Journal of the Linnean Society.

The Tres Marías archipelago in the central Mexican Pacific is a protected area that has a complex geological history due to its tectonic setting. This study describes an integrative analysis of the biogeographical affinities of the biota inhabiting the islands. A biotic component analysis showed a close relationship between the islands and the Pacific Lowlands and Veracruzan biogeographical provinces, whereas a cladistic biogeographical analysis additionally showed a Nearctic affinity with the Sonoran biogeographical province. The biogeographical affinity patterns, based on the distribution of the sister group of each endemic species, revealed three distinct patterns: Neotropical, Sonoran-Neotropical and Nearctic-Neotropical. The study recognized that the Tres Marías Islands are a region of great biological complexity where the biota of the Pacific Lowlands and the Veracruzan provinces intersect, with a predominantly Neotropical affinity. In this biogeographical analysis, information on the biotic assemblage and the geological history of the Tres Marías Islands are integrated and discussed. The biotic assembly of the islands must have occurred via both vicariance and dispersal at different geological times, related to opening of the Gulf of California (Miocene–Pleistocene) as well as to periods of glaciation (Pleistocene).

Kudoh, A., J. P. Megonigal, J. A. Langley, G. L. Noyce, T. Sakai, and D. F. Whigham. 2023. Reproductive Responses to Increased Shoot Density and Global Change Drivers in a Widespread Clonal Wetland Species, Schoenoplectus americanus. Estuaries and Coasts.

The expansion of many wetland species is a function of both clonal propagation and sexual reproduction. The production of ramets through clonal propagation enables plants to move and occupy space near parent ramets, while seeds produced by sexual reproduction enable species to disperse and colonize open or disturbed sites both near and far from parents. The balance between clonal propagation and sexual reproduction is known to vary with plant density but few studies have focused on reproductive allocation with density changes in response to global climate change. Schoenoplectus americanus is a widespread clonal wetland species in North America and a dominant species in Chesapeake Bay brackish tidal wetlands. Long-term experiments on responses of S . americanus to global change provided the opportunity to compare the two modes of propagation under different treatments. Seed production increased with increasing shoot density, supporting the hypothesis that factors causing increased clonal reproduction (e.g., higher shoot density) stimulate sexual reproduction and dispersal of genets. The increase in allocation to sexual reproduction was mainly the result of an increase in the number of ramets that flowered and not an increase in the number of seeds per reproductive shoot, or the ratio between the number of flowers produced per inflorescence and the number of flowers that developed into seeds. Seed production increased in response to increasing temperatures and decreased or did not change in response to increased CO 2 or nitrogen. Results from this comparative study demonstrate that plant responses to global change treatments affect resource allocation and can alter the ability of species to produce seeds.

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.

de Deus Vidal, J., C. B. Schmitt, and I. Koch. 2023. Comparative richness patterns of range sizes and life forms of Apocynaceae along forest–savanna transitions in Brazil. Botanical Journal of the Linnean Society.

Brazilian moist forests and savannas are some of the most species-rich biomes in the Neotropics. In the transition zones between these regions, ecotones often accumulate even higher taxonomic diversity. However, whether these ecotonal communities consist of overlapping species widespread from the neighbouring biomes or a specific set of locally adapted species still needs to be clarified. Regional differences in species richness may be influenced by factors such as species' environmental tolerances, life forms, or species’ range sizes. To investigate the species richness found in ecotones, we used the ‘milk-weed’ family (Apocynaceae), which comprises both widespread and narrowly distributed trees, lianas, and shrubs, as a model to evaluate if (i) their observed richness in ecotones is promoted by widespread species or by locally adapted species; (ii) trees, lianas, and shrubs show different richness patterns in savannas, ecotones, and forests; and (iii) species found in ecotones have broader environmental tolerances than other species in the family. We used a taxonomically curated georeferenced dataset to compare the range sizes of 643 species of Apocynaceae from 73 genera listed for Brazil, comprising 298 species with a liana life form and 345 trees, herbs, or shrubs. We recorded 335 predominantly forest species, 56 savanna species, and 152 ecotone species, for which we quantified species richness, areas of occurrence, precipitation, and temperature ranges and tested for differences in range sizes and environmental tolerances between habits and ecoregions. Our results indicate that (i) Apocynaceae species occurring in ecotones have wider geographical ranges than species not occurring in ecotones; (ii) lianas showed higher area-weighted richness in ecotones than other life forms; and (iii) species found in ecotones had broader environmental tolerances than species restricted to moist forests or savannas. These results indicate that the species richness found in ecotones between savannas and moist forests in Brazil is not necessarily a consequence of higher endemism and local adaptation but may also be a result of overlapping ranges of widespread species typically associated with neighbouring biomes. Together, our findings add to our understanding of ecotones and biomes as continuous, gradual biogeographical transitions instead of sharply defined ecological units.