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.

Rayos, A. L., M. A. M. Renner, and S. Y. W. Ho. 2024. The Neotropical endemic liverwort subfamily Micropterygioideae had circum‐Antarctic links to the rest of the Lepidoziaceae during the early Cretaceous. Ecology and Evolution 14. https://doi.org/10.1002/ece3.11066

Lepidoziaceae are the third‐largest family of liverworts, with about 860 species distributed on all continents. The evolutionary history of this family has not been satisfactorily resolved, with taxa such as Micropterygioideae yet to be included in phylogenetic analyses. We inferred a dated phylogeny of Lepidoziaceae using a data set consisting of 13 genetic markers, sampled from 147 species. Based on our phylogenetic estimate, we used statistical dispersal‐vicariance analysis to reconstruct the biogeographic history of the family. We inferred a crown age of 197 Ma (95% credible interval 157–240 Ma) for the family in the Australian region, with most major lineages also originating in the same region. Micropterygioideae are placed as the sister group to Lembidioideae, with these two lineages diverging from each other about 132 Ma in the South American–Australian region. With South America and Australia being connected through Antarctica at the time, our results suggest a circum‐Antarctic link between Micropterygioideae and the rest of the family. Crown Micropterygioideae were inferred to have arisen 45 Ma in South America before the continent separated from Antarctica. Extinction from southern temperate regions might explain the present‐day restriction of Micropterygioideae to the Neotropics. Our study reveals the influence of past geological events, such as continental drift, on the evolution and distribution of a widespread and diverse family of liverworts.

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.

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. https://doi.org/10.1111/nph.19601

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.

Minghetti, E., P. M. Dellapé, M. Maestro, and S. I. Montemayor. 2024. Evaluating the climatic suitability of Engytatus passionarius Minghetti et al. (Heteroptera, Miridae) as a biological control agent of the invasive stinking passion flower Passiflora foetida L. in Australia through ecological niche models. Biological Control 191: 105461. https://doi.org/10.1016/j.biocontrol.2024.105461

Passiflora foetida is a climbing vine, native to the Neotropical Region that is causing major economic and ecological damage in Australia, where it is rapidly spreading. Traditional control options, such as cutting, manual uprooting, and herbicide applications are only effective for local management. Currently, the plant bug Engytatus passionarius is the most promising biological control agent. Specificity tests performed in its native range in Argentina suggest it is highly specific to the plant, and it has not been observed in the field associated with other plants. As climate determines the establishment of insects, knowing if the environmental conditions suit their requirements is key to introducing a species in a region. Also, an overlap between the climatic niches of species is an indicator of similar requirements. To explore the possibilities of a successful establishment of E. passionarius in Australia, ecological niche models (ENM) were built for the plant bug and for the vine and their overlap was measured. The ENM projected to Australia recognized suitable environmental conditions for the establishment of E. passionarius in several regions where P. foetida is present, both for current and future scenarios. Moreover, the niche of the plant bug is almost completely overlapped with that of the vine. All the aforementioned evidence seems to indicate that E. passionarius has a good chance to become an effective biological control agent of P. foetida.

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.

Angulo, J. C., J. M. Burke, and F. A. Michelangeli. 2023. Characterizing the frequency, morphological gradient, and distribution of dioecy in Miconia (Melastomataceae). International Journal of Plant Sciences. https://doi.org/10.1086/729063

Dioecy has evolved many times independently within the angiosperms. The distribution, frequency of occurrence, and floral morphology of dioecious angiosperms constitute the foundations for comparative studies of dioecy, yet for many groups they are still poorly characterized. We assessed species of Miconia for the presence of dioecious reproductive system, characterized the floral morphology for staminate and pistillate flowers, and used herbarium records to analyze patterns of distribution and elevational range. We find that dioecious Miconia represent an uncommon case of mismatched stage of organ abortion between staminate and pistillate flowers, with functionally pistillate flower morphology largely consistent across species, and morphological expression in functionally staminate flowers varying from near absent to slight reductions in gynoecia. We identify 58 dioecious species and 15 putatively dioecious species within Miconia that are distributed primarily in montane habitats between 1000 m – 3500 m in the Andes, parts of Central America, and the Caribbean. Our results double the last known count of dioecy in Miconia and highlight the gradient of vestigial morphology in staminate flowers. Lastly, we provide discussion on the significance of dioecy in relation to floral development, pollination, and ecology in Miconia.

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.

McCulloch-Jones, E. J., T. Kraaij, N. Crouch, and K. T. Faulkner. 2023. Assessing the invasion risk of traded alien ferns using species distribution models. NeoBiota 87: 161–189. https://doi.org/10.3897/neobiota.87.101104

Risk analysis plays a crucial role in regulating and managing alien and invasive species but can be time-consuming and costly. Alternatively, combining invasion and impact history with species distribution models offers a cost-effective and time-efficient approach to assess invasion risk and identify species for which a comprehensive risk analysis should take precedence. We conducted such an assessment for six traded alien fern species, determining their invasion risk in countries where they are traded. Four of the species (Dicksonia antarctica, Dryopteris erythrosora, Lygodium japonicum, and Phlebodium aureum) showed limited global distributions, while Adiantum raddianum and Sphaeropteris cooperi had broader distributions. A. raddianum, however, was the only species found to pose a high invasion risk in two known trade countries – the USA and Australia – and requires a complete risk analysis to determine the appropriate regulatory responses. Dicksonia antarctica, Phlebodium aureum (for New Zealand), and Dryopteris erythrosora (for the USA) posed a medium risk of invasion due to the lack of evidence of impacts, and a complete risk analysis is thus deemed less crucial for these species in these countries. For other species, suitable environments were not predicted in the countries where they are traded, thus the risk of invasion is low, and a complete risk analysis is not required. For species in countries where suitable environments are predicted but no trade information or presence data are available, risk assessments are recommended to better determine the risk posed. Despite the relatively limited potential global distribution of the studied ferns relative to other major plant invaders (e.g., Pinus spp. and Acacia spp.), their history of invasion, documented impacts in pristine environments, and high propagule pressure from trade warrants concern, possibly necessitating legislative and regulatory measures in environmentally suitable regions.

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.