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. https://doi.org/10.1093/evolut/qpae034

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. 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.

Short, A. W., J. S. V. Sebastian, J. Huang, G. Wang, M. Dassanayake, P. M. Finnegan, J. D. Parker, et al. 2024. Comparative transcriptomics of the chilling stress response in two Asian mangrove species Bruguiera gymnorhiza and Rhizophora apiculata. Tree Physiology. https://doi.org/10.1093/treephys/tpae019

Abstract Low temperatures largely determine the geographic limits of plant species by reducing survival and growth. Interspecific differences in the geographic distribution of mangrove species have been associated with cold tolerance, with exclusively tropical species being highly cold-sensitive and subtropical species being relatively cold-tolerant. To identify species-specific adaptations to low temperatures, we compared the chilling stress response of two widespread Indo-West Pacific mangrove species from Rhizophoraceae with differing latitudinal range limits—Bruguiera gymnorhiza (subtropical range limit) and Rhizophora apiculata (tropical range limit). For both species, we measured the maximum photochemical efficiency of photosystem II (Fv/Fm) as a proxy for the physiological condition of the plants and examined gene expression profiles during chilling at 15 °C and 5 °C. At 15 °C, B. gymnorhiza maintained a significantly higher Fv/Fm than R. apiculata. However, at 5 °C, both species displayed equivalent Fv/Fm values. Thus, species-specific differences in chilling tolerance were only found at 15 °C, and both species were sensitive to chilling at 5 °C. At 15 °C, B. gymnorhiza down-regulated genes related to the light reactions of photosynthesis and up-regulated a gene involved in cyclic electron flow regulation, while R. apiculata down-regulated more RuBisCo related genes. At 5 °C, both species repressed genes related to CO2 assimilation. The down-regulation of genes related to light absorption and up-regulation of genes related to cyclic electron flow regulation are photoprotective mechanisms that likely contributed to the greater PSII photochecmical efficiency of B. gymnorhiza at 15 °C. The results of this study provide evidence that the distributional range limits and potentially the expansion rates of plant species are associated with differences in the regulation of photosynthesis and photoprotective mechanisms under low temperatures.

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.

Groh, S. S., P. Upchurch, J. J. Day, and P. M. Barrett. 2023. The biogeographic history of neosuchian crocodiles and the impact of saltwater tolerance variability. Royal Society Open Science 10. https://doi.org/10.1098/rsos.230725

Extant neosuchian crocodiles are represented by only 24 taxa that are confined to the tropics and subtropics. However, at other intervals during their 200 Myr evolutionary history the clade reached considerably higher levels of species-richness, matched by more widespread distributions. Neosuchians have occupied numerous habitats and niches, ranging from dwarf riverine forms to large marine predators. Despite numerous previous studies, several unsolved questions remain with respect to their biogeographic history, including the geographical origins of major groups, e.g. Eusuchia and Neosuchia itself. We carried out the most comprehensive biogeographic analysis of Neosuchia to date, based on a multivariate K-means clustering approach followed by the application of two ancestral area estimation methods (BioGeoBEARS and Bayesian ancestral location estimation) applied to two recently published phylogenies. Our results place the origin of Neosuchia in northwestern Pangaea, with subsequent radiations into Gondwana. Eusuchia probably emerged in the European archipelago during the Late Jurassic/Early Cretaceous, followed by dispersals to the North American and Asian landmasses. We show that putative transoceanic dispersal events are statistically significantly less likely to happen in alligatoroids. This finding is consistent with the saltwater intolerant physiology of extant alligatoroids, bolstering inferences of such intolerance in their ancestral lineages.

ter Huurne, M. B., L. J. Potgieter, C. Botella, and D. M. Richardson. 2023. Melaleuca (Myrtaceae): Biogeography of an important genus of trees and shrubs in a changing world. South African Journal of Botany 162: 230–244. https://doi.org/10.1016/j.sajb.2023.08.052

The number of naturalised and invasive woody plant species has increased rapidly in recent decades. Despite the increasing interest in tree and shrub invasions, little is known about the invasion ecology of most species. This paper explores the global movement of species in the genus Melaleuca (Myrtaceae; here including the genus Callistemon). We assess the global introduction history, distribution and biogeographic status of the genus. Various global species occurrence databases, citizen science (iNaturalist), and the literature were used.Seventy-two species [out of 386 Melaleuca species; 19%] have been introduced to at least 125 regions outside their native range. The main regions of global Melaleuca introductions are Southeast Asia, the southern parts of North America, south-eastern South America, southern Africa and Europe. The earliest record of a Melaleuca species outside of the native range of the genus is 1789. First records of Melaleuca species outside their native range were most commonly recorded in the 1960s, with records from all over the world. The main reasons for Melaleuca introductions were for use in the tea tree (pharmaceutical value) and ornamental horticulture industries. Melaleuca introductions, naturalizations and invasions are recent compared to many other woody plant taxa. Experiences in Florida and South Africa highlight the potential of Melaleuca species to spread rapidly and have significant ecological impacts. It is likely that the accumulating invasion debt will result in further naturalization and invasion of Melaleuca species in the future.

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.

Li, Y., F. Ding, M. Hao, S. Chen, D. Jiang, P. Fan, Y. Qian, et al. 2023. The implications for potential marginal land resources of cassava across worldwide under climate change challenges. Scientific Reports 13. https://doi.org/10.1038/s41598-023-42132-y

The demand for energy plants is foreseen to grow as worldwide energy and climate policies promote the use of bioenergy for climate change mitigation. To avoid competing with food production, it’s critical to assess future changes in marginal land availability for energy plant development. Using a machine learning method, boosted regression tree, this study modeled potential marginal land resources suitable for cassava under current and different climate change scenarios, based on cassava occurrence records and environmental covariates. The findings revealed that, currently, over 80% of the 1357.24 Mha of available marginal land for cassava cultivation is distributed in Africa and South America. Under three climate change scenarios, by 2030, worldwide suitable marginal land resources were predicted to grow by 39.71Mha, 66.21 Mha, and 39.31Mha for the RCP4.5, RCP6.0, and RCP8.5 scenarios, respectively; by 2050, the potential marginal land suitable for cassava will increase by 38.98Mha, 83.02 Mha, and 55.43Mha, respectively; by 2080, the global marginal land resources were estimated to rise by 40.82 Mha, 99.74 Mha, and 21.87 Mha from now, respectively. Our results highlight the impacts of climate change on potential marginal land resources of cassava across worldwide, which provide the basis for assessing bioenergy potential in the future.

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. https://doi.org/10.3390/plants12173069

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. https://doi.org/10.1002/ajb2.16235

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.