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Science Enabled by Specimen Data

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. https://doi.org/10.1093/botlinnean/boad009

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.

Medzihorský, V., J. Trombik, R. Mally, M. Turčáni, and A. M. Liebhold. 2023. Insect invasions track a tree invasion: Global distribution of black locust herbivores. Journal of Biogeography. https://doi.org/10.1111/jbi.14625

Aim Many invasive plant species benefit from enemy release resulting from the absence of insect herbivores in their invaded range. However, over time, specialized herbivores may ‘catch up’ with such invasive plants. Black locust is a tree species with a relatively limited native range in North America but has invaded large areas in virtually every temperate continent including North America. We hypothesize that both intra- and intercontinental spread of black locust leads to a parallel, though delayed pattern of intra- and intercontinental spread of insect herbivores. Location Global. Taxon Black locust, Robinia pseudoacacia, and its insect herbivores. Methods We compiled historical records of the occurrence of insect herbivore species associated with R. pseudoacacia from all world regions. Based on this list, we describe taxonomic patterns and investigate associations between environmental features and numbers of non-native specialist herbivores in the portion of North America invaded by R. pseudoacacia. Results A total of 454 herbivorous species are recorded feeding on R. pseudoacacia across the world, with 23 of these being specialized on Robinia. From this group, seven species have successfully expanded their range beyond North America. Within North America, the richness of specialists is explained by a combination of road density, R. pseudoacacia density, distance from the R. pseudoacacia native range, and climate. Main Conclusion Non-native herbivore species have accumulated on invasive R. pseudoacacia in both North America and in other continents. The steady build-up of invasions likely has diminished the enemy release that this invasive tree species has benefited from – a trend that will likely continue in the future. These findings support the hypothesis that invasive plants promote parallel though delayed invasions of specialist insect herbivores.

Clemente, K. J. E., and M. S. Thomsen. 2023. High temperature frequently increases facilitation between aquatic foundation species: a global meta‐analysis of interaction experiments between angiosperms, seaweeds, and bivalves. Journal of Ecology. https://doi.org/10.1111/1365-2745.14101

Many studies have quantified ecological impacts of individual foundation species (FS). However, emerging data suggest that FS often co‐occur, potentially inhibiting or facilitating one another, thereby causing indirect, cascading effects on surrounding communities. Furthermore, global warming is accelerating, but little is known about how interactions between co‐occurring FS vary with temperature.Shallow aquatic sedimentary systems are often dominated by three types of FS: slower‐growing clonal angiosperms, faster‐growing solitary seaweeds, and shell‐forming filter‐ and deposit‐feeding bivalves. Here, we tested the impacts of one FS on another by analyzing manipulative interaction experiments from 148 papers with a global meta‐analysis.We calculated 1,942 (non‐independent) Hedges’ g effect sizes, from 11,652 extracted values over performance responses, such as abundances, growths or survival of FS, and their associated standard deviations and replication levels. Standard aggregation procedures generated 511 independent Hedges’ g that was classified into six types of reciprocal impacts between FS.We found that (i) seaweeds had consistent negative impacts on angiosperms across performance responses, organismal sizes, experimental approaches, and ecosystem types; (ii) angiosperms and bivalves generally had positive impacts on each other (e.g., positive effects of angiosperms on bivalves were consistent across organismal sizes and experimental approaches, but angiosperm effect on bivalve growth and bivalve effect on angiosperm abundance were not significant); (iii) bivalves positively affected seaweeds (particularly on growth responses); (iv) there were generally no net effects of seaweeds on bivalves (except for positive effect on growth) or angiosperms on seaweeds (except for positive effect on ‘other processes’); and (v) bivalve interactions with other FS were typically more positive at higher temperatures, but angiosperm‐seaweed interactions were not moderated by temperature.Synthesis: Despite variations in experimental and spatiotemporal conditions, the stronger positive interactions at higher temperatures suggest that facilitation, particularly involving bivalves, may become more important in a future warmer world. Importantly, addressing research gaps, such as the scarcity of FS interaction experiments from tropical and freshwater systems and for less studied species, as well as testing for density‐dependent effects, could better inform aquatic ecosystem conservation and restoration efforts and broaden our knowledge of FS interactions in the Anthropocene.

Huang, T., J. Chen, K. E. Hummer, L. A. Alice, W. Wang, Y. He, S. Yu, et al. 2023. Phylogeny of Rubus (Rosaceae): Integrating molecular and morphological evidence into an infrageneric revision. TAXON. https://doi.org/10.1002/tax.12885

Rubus (Rosaceae), one of the most complicated angiosperm genera, contains about 863 species, and is notorious for its taxonomic difficulty. The most recent (1910–1914) global taxonomic treatment of the genus was conducted by Focke, who defined 12 subgenera. Phylogenetic results over the past 25 years suggest that Focke's subdivisions of Rubus are not monophyletic, and large‐scale taxonomic revisions are necessary. Our objective was to provide a comprehensive phylogenetic analysis of the genus based on an integrative evidence approach. Morphological characters, obtained from our own investigation of living plants and examination of herbarium specimens are combined with chloroplast genomic data. Our dataset comprised 196 accessions representing 145 Rubus species (including cultivars and hybrids) and all of Focke's subgenera, including 60 endemic Chinese species. Maximum likelihood analyses inferred phylogenetic relationships. Our analyses concur with previous molecular studies, but with modifications. Our data strongly support the reclassification of several subgenera within Rubus. Our molecular analyses agree with others that only R. subg. Anoplobatus forms a monophyletic group. Other subgenera are para‐ or polyphyletic. We suggest a revised subgeneric framework to accommodate monophyletic groups. Character evolution is reconstructed, and diagnostic morphological characters for different clades are identified and discussed. Based on morphological and molecular evidence, we propose a new classification system with 10 subgenera: R. subg. Anoplobatus, R. subg. Batothamnus, R. subg. Chamaerubus, R. subg. Cylactis, R. subg. Dalibarda, R. subg. Idaeobatus, R. subg. Lineati, R. subg. Malachobatus, R. subg. Melanobatus, and R. subg. Rubus. The revised infrageneric nomenclature inferred from our analyses is provided along with synonymy and type citations. Our new taxonomic backbone is the first systematic and complete global revision of Rubus since Focke's treatment. It offers new insights into deep phylogenetic relationships of Rubus and has important theoretical and practical significance for the development and utilization of these important agronomic crops.

Sumbembayev, A. A., S. Nowak, A. Burzacka-Hinz, A. Kosiróg-Ceynowa, and D. L. Szlachetko. 2023. New and Noteworthy Taxa of the Genus Dactylorhiza Necker ex Nevski (Orchidaceae Juss.) in Kazakhstan Flora and Its Response to Global Warming. Diversity 15: 369. https://doi.org/10.3390/d15030369

A critical study of the herbarium material representing the orchid genus Dactylorhiza Necker ex Nevski in Kazakhstan was conducted in 2019–2020. The information on the species composition was clarified. Dactylorhiza fuchsii subsp. hebridensis (Wilmott) Soó and D. × kerneri (Soó) Soó were identified for the first time in the country. New taxa were noted for individual botanical and geographical areas. All taxa were presented in the list and annotated with studied herbarium materials from the Kazakhstan area. Based on the collected and available locations for the studied taxa, distribution modeling was carried out for the four taxa (D. incarnata, D. majalis subsp. baltica, D. salina, and D. umbrosa). Bioclimatic data for the present and future (2041–2060) based on four possible scenarios were used. The occurrence of Dactylorhiza representatives in Kazakhstan is threatened by global climate warming. It is likely that some of them may not occur in the country in the future (D. incarnata and D. majalis subsp. baltica), losing up to 99.87% of their modern range or their range may be significantly reduced (D. salina and D. umbrosa), losing up to 80.83% of their present distribution. It is worth considering global changes in planning conservation activities and identifying areas that may play a significant role in the functioning of the national flora in the future.

Denk, T., G. W. Grimm, A. L. Hipp, J. M. Bouchal, E.-D. Schulze, and M. C. Simeone. 2023. Niche evolution in a northern temperate tree lineage: biogeographic legacies in cork oaks (Quercus sect. Cerris). Annals of Botany. https://doi.org/10.1093/aob/mcad032

Abstract Background and Aims Cork oaks (Quercus sect. Cerris) comprise 15 extant species in Eurasia. Despite being a small clade, they display a range of leaf morphologies comparable to the largest sections (>100 spp.) in Quercus. Their fossil record extends back to the Eocene. Here, we explore how cork oaks achieved their modern ranges and how legacy effects may explain niche evolution in modern species of section Cerris and its sister section Ilex, the holly oaks. Methods We inferred a dated phylogeny for cork and holly oaks using a reduced-representation next-generation sequencing method, restriction-site associated DNA sequencing (RAD-seq) and used D-statistics to investigate gene flow hypotheses. We estimated divergence times using a fossilized birth-death (FBD) model calibrated with 47 fossils. We used Köppen profiles, selected bioclimatic parameters, and forest biomes occupied by modern species to infer ancestral climatic and biotic niches. Key Results East Asian and Western Eurasian cork oaks diverged initially in the Eocene. Subsequently, four Western Eurasian lineages (subsections) differentiated during the Oligocene and Miocene. Evolution of leaf size, form, and texture partly correlates with multiple transitions from ancestral humid temperate climates to Mediterranean, arid, and continental climates. Distantly related but ecologically similar species converged on similar leaf traits in the process. Conclusions Originating in temperate (frost-free) biomes, Eocene to Oligocene ranges of the primarily deciduous cork oaks were restricted to higher latitudes (Siberia to north of Paratethys). Members of the evergreen holly oaks (sect. Ilex) also originated in temperate biomes but migrated south- and south-westwards into then-(sub)tropical southern China and south-eastern Tibet during the Eocene, then westwards along existing pre-Himalayan mountain ranges. Divergent biogeographic histories and deep-time phylogenetic legacies—in cold and drought tolerance, nutrient storage, and fire resistance—thus account for the modern species mosaic of Western Eurasian oak communities, which comprise oaks belonging to four sections.

Reichgelt, T., A. Baumgartner, R. Feng, and D. A. Willard. 2023. Poleward amplification, seasonal rainfall and forest heterogeneity in the Miocene of the eastern USA. Global and Planetary Change 222: 104073. https://doi.org/10.1016/j.gloplacha.2023.104073

Paleoclimate reconstructions can provide a window into the environmental conditions in Earth history when atmospheric carbon dioxide concentrations were higher than today. In the eastern USA, paleoclimate reconstructions are sparse, because terrestrial sedimentary deposits are rare. Despite this, the eastern USA has the largest population and population density in North America, and understanding the effects of current and future climate change is of vital importance. Here, we provide terrestrial paleoclimate reconstructions of the eastern USA from Miocene fossil floras. Additionally, we compare proxy paleoclimate reconstructions from the warmest period in the Miocene, the Miocene Climatic Optimum (MCO), to those of an MCO Earth System Model. Reconstructed Miocene temperatures and precipitation north of 35°N are higher than modern. In contrast, south of 35°N, temperatures and precipitation are similar to today, suggesting a poleward amplification effect in eastern North America. Reconstructed Miocene rainfall seasonality was predominantly higher than modern, regardless of latitude, indicating greater variability in intra-annual moisture transport. Reconstructed climates are almost uniformly in the temperate seasonal forest biome, but heterogeneity of specific forest types is evident. Reconstructed Miocene terrestrial temperatures from the eastern USA are lower than modeled temperatures and coeval Atlantic sea surface temperatures. However, reconstructed rainfall is consistent with modeled rainfall. Our results show that during the Miocene, climate was most different from modern in the northeastern states, and may suggest a drastic reduction in the meridional temperature gradient along the North American east coast compared to today.

Wilson Brown, M. K., and E. B. Josephs. 2023. Evaluating niche changes during invasion with seasonal models in Capsella bursa‐pastoris. American Journal of Botany. https://doi.org/10.1002/ajb2.16140

Premise Researchers often use ecological niche models to predict where species might establish and persist under future or novel climate conditions. However, these predictive methods assume species have stable niches across time and space. Furthermore, ignoring the time of occurrence data can obscure important information about species reproduction and ultimately fitness. Here, we assess compare ecological niche models generated from full-year averages to seasonal models Methods In this study, we generate full-year and monthly ecological niche models for Capsella bursa-pastoris in Europe and North America to see if we can detect changes in the seasonal niche of the species after long-distance dispersal. Key Results We find full-year ecological niche models have low transferability across continents and there are continental differences in the climate conditions that influence the distribution of C. bursa-pastoris. Monthly models have greater predictive accuracy than full-year models in cooler seasons, but no monthly models are able to predict North American summer occurrences very well. Conclusions The relative predictive ability of European monthly models compared to North American monthly models suggests a change in the seasonal timing between the native range to the non-native range. These results highlight the utility of ecological niche models at finer temporal scales in predicting species distributions and unmasking subtle patterns of evolution.

Pan, Y., J. García-Girón, and L. L. Iversen. 2023. Global change and plant-ecosystem functioning in freshwaters. Trends in Plant Science. https://doi.org/10.1016/j.tplants.2022.12.013

Freshwater ecosystems are of worldwide importance for maintaining biodiversity and sustaining the provision of a myriad of ecosystem services to modern societies. Plants, one of the most important components of these ecosystems, are key to water nutrient removal, carbon storage, and food provision. Understanding how the functional connection between freshwater plants and ecosystems is affected by global change will be key to our ability to predict future changes in freshwater systems. Here, we synthesize global plant responses, adaptations, and feedbacks to present-day and future freshwater environments through trait-based approaches, from single individuals to entire communities. We outline the transdisciplinary knowledge benchmarks needed to further understand freshwater plant biodiversity and the fundamental services they provide.

Aguirre‐Liguori, J. A., A. Morales‐Cruz, and B. S. Gaut. 2022. Evaluating the persistence and utility of five wild Vitis species in the context of climate change. Molecular Ecology. https://doi.org/10.1111/mec.16715

Crop wild relatives (CWRs) have the capacity to contribute novel traits to agriculture. Given climate change, these contributions may be especially vital for the persistence of perennial crops, because perennials are often clonally propagated and consequently do not evolve rapidly. By studying the landscape genomics of samples from five Vitis CWRs (V. arizonica, V. mustangensis, V. riparia, V. berlandieri and V. girdiana) in the context of projected climate change, we addressed two goals. The first was to assess the relative potential of different CWR accessions to persist in the face of climate change. By integrating species distribution models with adaptive genetic variation, additional genetic features such as genomic load and a phenotype (resistance to Pierce’s Disease), we predicted that accessions from one species (V. mustangensis) are particularly well‐suited to persist in future climates. The second goal was to identify which CWR accessions may contribute to bioclimatic adaptation for grapevine (V. vinifera) cultivation. To do so, we evaluated whether CWR accessions have the allelic capacity to persist if moved to locations where grapevines (V. vinifera) are cultivated in the United States. We identified six candidates from V. mustangensis and hypothesized that they may prove useful for contributing alleles that can mitigate climate impacts on viticulture. By identifying candidate germplasm, this work takes a conceptual step toward assessing the genomic and bioclimatic characteristics of CWRs.