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.

Cosme, M. 2023. Mycorrhizas drive the evolution of plant adaptation to drought. Communications Biology 6. https://doi.org/10.1038/s42003-023-04722-4

Plant adaptation to drought facilitates major ecological transitions, and will likely play a vital role under looming climate change. Mycorrhizas, i.e. strategic associations between plant roots and soil-borne symbiotic fungi, can exert strong influence on the tolerance to drought of extant plants. Here, I show how mycorrhizal strategy and drought adaptation have been shaping one another throughout the course of plant evolution. To characterize the evolutions of both plant characters, I applied a phylogenetic comparative method using data of 1,638 extant species globally distributed. The detected correlated evolution unveiled gains and losses of drought tolerance occurring at faster rates in lineages with ecto- or ericoid mycorrhizas, which were on average about 15 and 300 times faster than in lineages with the arbuscular mycorrhizal and naked root (non-mycorrhizal alone or with facultatively arbuscular mycorrhizal) strategy, respectively. My study suggests that mycorrhizas can play a key facilitator role in the evolutionary processes of plant adaptation to critical changes in water availability across global climates. Phylogenetic comparative analysis using data of 1,638 species of angiosperms and gymnosperms suggests that the evolution of plant adaptation to critical environmental change in water availability across global climates is dependent on mycorrhizas.

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.

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.

Baltensperger, A., J. Hagelin, P. Schuette, A. Droghini, and K. Ott. 2022. High dietary and habitat diversity indicate generalist behaviors of northern bog lemmings Synaptomys borealis in Alaska, USA. Endangered Species Research 49: 145–158. https://doi.org/10.3354/esr01211

The northern bog lemming Synaptomys borealis (NBL) is a rare small mammal that is undergoing a federal Species Status Assessment (SSA) under the US Endangered Species Act. Despite a wide North American distribution, very little is known about NBL dietary or habitat needs, both of which are germane to the resiliency of this species to climate change. To quantify diet composition of NBL in Alaska, we used DNA metabarcoding from 59 archived specimens to describe the taxonomic richness and relative abundance of foods in recent diets. DNA analyses revealed a broad diet composed of at least 110 families and 92 genera of bryophytes (mosses and liverworts), graminoids, fungi, forbs, and woody shrubs. Nine bryophyte genera and Carex sedges composed the largest portions of NBL diets. To quantify habitat preference, we intersected 467 georeferenced occurrence records of NBL in Alaska with remotely sensed land cover classes and used a compositional analysis framework that accounts for the relative abundance of land cover types. We did not detect significant habitat preferences for specific land cover types, although NBL frequently occurred in evergreen forest, woody wetlands, and adjacent to water. Our research highlights the importance of bryophytes, among a high diversity of dietary components, and describes NBL as boreal habitat generalists. Results will inform the current federal SSA by quantifying the extent to which ecological constraints are likely to affect NBL in a rapidly changing boreal environment.

Kroonen, G., A. Jakob, A. I. Palmér, P. van Sluis, and A. Wigman. 2022. Indo-European cereal terminology suggests a Northwest Pontic homeland for the core Indo-European languages S. Wichmann [ed.],. PLOS ONE 17: e0275744. https://doi.org/10.1371/journal.pone.0275744

Questions on the timing and the center of the Indo-European language dispersal are central to debates on the formation of the European and Asian linguistic landscapes and are deeply intertwined with questions on the archaeology and population history of these continents. Recent palaeogenomic studies support scenarios in which the core Indo-European languages spread with the expansion of Early Bronze Age Yamnaya herders that originally inhabited the East European steppes. Questions on the Yamnaya and Pre-Yamnaya locations of the language community that ultimately gave rise to the Indo-European language family are heavily dependent on linguistic reconstruction of the subsistence of Proto-Indo-European speakers. A central question, therefore, is how important the role of agriculture was among the speakers of this protolanguage. In this study, we perform a qualitative etymological analysis of all previously postulated Proto-Indo-European terminology related to cereal cultivation and cereal processing. On the basis of the evolution of the subsistence strategies of consecutive stages of the protolanguage, we find that one or perhaps two cereal terms can be reconstructed for the basal Indo-European stage, also known as Indo-Anatolian, but that core Indo-European, here also including Tocharian, acquired a more elaborate set of terms. Thus, we linguistically document an important economic shift from a mostly non-agricultural to a mixed agro-pastoral economy between the basal and core Indo-European speech communities. It follows that the early, eastern Yamnaya of the Don-Volga steppe, with its lack of evidence for agricultural practices, does not offer a perfect archaeological proxy for the core Indo-European language community and that this stage of the language family more likely reflects a mixed subsistence as proposed for western Yamnaya groups around or to the west of the Dnieper River.

Gougherty, A. V., S. R. Keller, and M. C. Fitzpatrick. 2022. Do genetically informed distribution models improve range predictions in past climates? A case study with balsam poplar. Frontiers of Biogeography 14. https://doi.org/10.21425/f5fbg56931

Species distribution models (SDMs) are one of the most widely used approaches to predict changes in habitat suitability in response to climate change. However, as typically implemented, SDMs treat species as genetically uniform throughout their ranges and thereby ignore potentially important genetic differences between populations. While numerous studies have used SDMs to model genetically based subgroupings within species, the ability of such models to be transferred to new times has rarely been evaluated. Here, we used standard and genetically informed distribution models (gSDMs) to predict the future and past range of balsam poplar (Populus balsamifera L.). We then assessed model transferability of standard SDMs and gSDMs using balsam poplar fossil pollen and macrofossil occurrences. In general, standard and gSDMs performed similarly through time, with both predicting a northward expanding range from refugia as glaciers receded over the past 22 ky BP and declining suitable area in future climates. Both standard and gSDMs showed moderate abilities to distinguish balsam poplar fossils from pseudo-absences but tended to predict lower suitability at fossil sites during the Pleistocene-Holocene transition. Although gSDMs applied to balsam poplar did not prove more transferable than standard SDMs, they provided numerous unique insights, such as the change in suitable area of genetic clusters through time and potential refugial locations. We argue more research is needed to determine which species may benefit most from the gSDM approach and to test gSDMs with temporally or spatially independent occurrences, as is often recommended for standard SDMs.

Marcussen, T., H. E. Ballard, J. Danihelka, A. R. Flores, M. V. Nicola, and J. M. Watson. 2022. A Revised Phylogenetic Classification for Viola (Violaceae). Plants 11: 2224. https://doi.org/10.3390/plants11172224

The genus Viola (Violaceae) is among the 40–50 largest genera among angiosperms, yet its taxonomy has not been revised for nearly a century. In the most recent revision, by Wilhelm Becker in 1925, the then-known 400 species were distributed among 14 sections and numerous unranked groups. Here, we provide an updated, comprehensive classification of the genus, based on data from phylogeny, morphology, chromosome counts, and ploidy, and based on modern principles of monophyly. The revision is presented as an annotated global checklist of accepted species of Viola, an updated multigene phylogenetic network and an ITS phylogeny with denser taxon sampling, a brief summary of the taxonomic changes from Becker’s classification and their justification, a morphological binary key to the accepted subgenera, sections and subsections, and an account of each infrageneric subdivision with justifications for delimitation and rank including a description, a list of apomorphies, molecular phylogenies where possible or relevant, a distribution map, and a list of included species. We distribute the 664 species accepted by us into 2 subgenera, 31 sections, and 20 subsections. We erect one new subgenus of Viola (subg. Neoandinium, a replacement name for the illegitimate subg. Andinium), six new sections (sect. Abyssinium, sect. Himalayum, sect. Melvio, sect. Nematocaulon, sect. Spathulidium, sect. Xanthidium), and seven new subsections (subsect. Australasiaticae, subsect. Bulbosae, subsect. Clausenianae, subsect. Cleistogamae, subsect. Dispares, subsect. Formosanae, subsect. Pseudorupestres). Evolution within the genus is discussed in light of biogeography, the fossil record, morphology, and particular traits. Viola is among very few temperate and widespread genera that originated in South America. The biggest identified knowledge gaps for Viola concern the South American taxa, for which basic knowledge from phylogeny, chromosome counts, and fossil data is virtually absent. Viola has also never been subject to comprehensive anatomical study. Studies into seed anatomy and morphology are required to understand the fossil record of the genus.

Ward, S. F., E. G. Brockerhoff, R. M. Turner, T. Yamanaka, L. Marini, S. Fei, and A. M. Liebhold. 2022. Prevalence and drivers of a tree-killing bark beetle, Ips typographus (Coleoptera, Scolytinae), in international invasion pathways into the USA. Journal of Pest Science. https://doi.org/10.1007/s10340-022-01559-4

The unintentional transport of insects beyond their native ranges has greatly increased with globalization over the past century, leading to higher propagule pressure in non-native ranges of many species. Knowledge about the prevalence of a species in international invasion pathways is important for predicting invasions and taking appropriate biosecurity measures. We investigated the spatiotemporal patterns and drivers of interceptions—detections of at least one individual with imported goods that potentially serve as a proxy for arrival rates—for a tree-killing bark beetle, the European spruce bark beetle ( Ips typographus L.; Coleoptera: Curculionidae: Scolytinae), in the USA from 1914 to 2008. Across the study period, there were 505 interceptions of I. typographus with shipments originating from > 25 countries at ports in 22 US states. Interceptions first occurred in 1938, peaked at 33 and 25 in 1984 and 1996, respectively, and declined after the mid-1990s. Interceptions of I. typographus did not have a statistically detectable relationship with outbreak levels in the native range, were inversely related to annual import volume (an artifact likely driven by changes in inspection policies), and were more frequent during the winter. Thus, while interceptions of I. typographus are challenging to predict, we found evidence that (i) biosecurity practices against this beetle could be increased during winter but not in response to outbreaks in source regions and (ii) the overall abundance of this beetle in invasion pathways has recently decreased, probably because strengthened phytosanitary protocols have reduced contamination levels and/or decreased the perceived need for inspections.