Science Enabled by Specimen Data

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.

Rosas, M. R., R. A. Segovia, and P. C. Guerrero. 2023. Climatic Niche Dynamics of the Astereae Lineage and Haplopappus Species Distribution following Amphitropical Long-Distance Dispersal. Plants 12: 2721. https://doi.org/10.3390/plants12142721

The tribe Astereae (Asteraceae) displays an American Amphitropical Disjunction. To understand the eco-evolutionary dynamics associated with a long-distance dispersal event and subsequent colonization of extratropical South America, we compared the climatic and geographic distributions of South American species with their closest North American relatives, focusing on the diverse South American Astereae genus, Haplopappus. Phylogenetic analysis revealed that two South American genera are closely related to seven North American genera. The climatic niche overlap (D = 0.5) between South and North America exhibits high stability (0.89), low expansion (0.12), and very low unfilling (0.04). The distribution of the North American species predicted the climatic and geographic space occupied by the South American species. In central Chile, Haplopappus showed a non-random latitudinal gradient in species richness, with Mediterranean climate variables mainly explaining the variation. Altitudinal patterns indicated peak richness at 600 m, declining at lower and higher elevations. These findings support climatic niche conservatism in shaping Haplopappus species distribution and diversity. Two major endemism zones were identified in central Chile and the southern region, with a transitional zone between Mediterranean and Temperate macro-bioclimates. Our results indicate strong niche conservatism following long-distance dispersal and slight niche expansion due to unique climatic variables in each hemisphere.

Graham, C. D. K., E. J. Forrestel, A. L. Schilmiller, A. T. Zemenick, and M. G. Weber. 2023. Evolutionary signatures of a trade-off in direct and indirect defenses across the wild grape genus Vitis. Evolution. https://doi.org/10.1093/evolut/qpad140

Evolutionary correlations between chemical defense and protection by mutualist bodyguards have been long predicted, but tests of these pattern remain rare. We use a phylogenetic framework to test for evolutionary correlations indicative of trade-offs or synergisms between direct defense in the form of plant secondary metabolism, and indirect defense in the form of leaf domatia, across 33 species in the wild grape genus, Vitis. We also performed a bioassay with a generalist herbivore to associate our chemical phenotypes with herbivore palatability. Finally, we tested whether defensive traits correlate with the average abiotic characteristics of each species’ contemporary range and whether these correlations were consistent with plant defense theory. We found a negative evolutionary correlation between domatia size and the diversity of secondary metabolites in Vitis leaf tissue across the genus, and also that leaves with a higher diversity and richness of secondary metabolites were less palatable to a generalist herbivore, consistent with a trade-off in chemical and mutualistic defense investment. Predictions from plant defense theory were not supported by associations between investment in defense phenotypes and abiotic variables. Our work demonstrates an evolutionary pattern indicative of a trade-off between indirect and direct defense strategies across the Vitis genus.

Shen, F., S. Xu, Q. Shen, C. Bi, and M. A. Lysak. 2023. The allotetraploid horseradish genome provides insights into subgenome diversification and formation of critical traits. Nature Communications 14. https://doi.org/10.1038/s41467-023-39800-y

Polyploidization can provide a wealth of genetic variation for adaptive evolution and speciation, but understanding the mechanisms of subgenome evolution as well as its dynamics and ultimate consequences remains elusive. Here, we report the telomere-to-telomere (T2T) gap-free reference genome of allotetraploid horseradish ( Armoracia rusticana ) sequenced using a comprehensive strategy. The (epi)genomic architecture and 3D chromatin structure of the A and B subgenomes differ significantly, suggesting that both the dynamics of the dominant long terminal repeat retrotransposons and DNA methylation have played critical roles in subgenome diversification. Investigation of the genetic basis of biosynthesis of glucosinolates (GSLs) and horseradish peroxidases reveals both the important role of polyploidization and subgenome differentiation in shaping the key traits. Continuous duplication and divergence of essential genes of GSL biosynthesis (e.g., FMO GS-OX , IGMT , and GH1 gene family) contribute to the broad GSL profile in horseradish. Overall, the T2T assembly of the allotetraploid horseradish genome expands our understanding of polyploid genome evolution and provides a fundamental genetic resource for breeding and genetic improvement of horseradish. Horseradish is a spicy root vegetable and it also produces horseradish peroxidase, an enzyme widely used in biochemistry applications. Here, the authors report its telomere-to-telomere reference genome, reveal subgenome diversification and the effect on the biosynthesis of glucosinolates and horseradish peroxidases.

Babin, C. H., and C. D. Bell. 2023. The effects of climate change on cytotype distributions of endemic genera in the North American Coastal Plain. Plant Ecology & Diversity. https://doi.org/10.1080/17550874.2023.2239244

Background Approximately 33% of plant species face extinction due to climate change. Polyploidisation, a process resulting in more than two complete sets of chromosomes, may be promoted by periods of climate fluctuations. Ecological niche modelling (ENM) using occurrences of endemic plants in the North American Coastal Plain (NACP) biodiversity hotspot could be used to evaluate the potential effects of climate change on cytotype distributions. Aims We used known diploid and polyploid taxa endemic to the NACP to test hypotheses that diploids and polyploids differed in habitat preferences, considerable overlap existed between cytotypes, and polyploid distributions would increase under climate change projections. Methods We examined niche identity and overlap of 28 congeneric ploidy level pairs and performed ENM to evaluate how climate change could affect these groups. Results Congeneric ploidy level pairs differed significantly in niche identity, and overlap varied across genera. Eleven genera showed greater than 100% increases in habitat suitability and six genera showed almost no remaining suitable habitat in at least one future climate scenario. Conclusions With 70% of the species that showed substantial declines in projected suitable habitat being of conservation concern, we propose that future studies of these genera should be a primary focus in the NACP.

Hill, A., M. F. T. Jiménez, N. Chazot, C. Cássia‐Silva, S. Faurby, L. Herrera‐Alsina, and C. D. Bacon. 2023. Apparent effect of range size and fruit colour on palm diversification may be spurious. Journal of Biogeography. https://doi.org/10.1111/jbi.14683

Aim Fruit selection by animal dispersers with different mobility directly impacts plant geographical range size, which, in turn, may impact plant diversification. Here, we examine the interaction between fruit colour, range size and diversification rate in palms by testing two hypotheses: (1) species with fruit colours attractive to birds have larger range sizes due to high dispersal ability and (2) disperser mobility affects whether small or large range size has higher diversification, and intermediate range size is expected to lead to the highest diversification rate regardless of disperser. Location Global. Time Period Contemporary (or present). Major Taxa Studied Palms (Arecaceae). Methods Palm species were grouped based on likely animal disperser group for given fruit colours. Range sizes were estimated by constructing alpha convex hull polygons from distribution data. We examined disperser group, range size or an interaction of both as possible drivers of change in diversification rate over time in a likelihood dynamic model (Several Examined State-dependent Speciation and Extinction [SecSSE]). Models were fitted, rate estimates were retrieved and likelihoods were compared to those of appropriate null models. Results Species with fruit colours associated with mammal dispersal had larger ranges than those with colours associated with bird dispersal. The best fitting SecSSE models indicated that the examined traits were not the primary driver of the heterogeneity in diversification rates in the model. Extinction rate complexity had a marked impact on model performance and on diversification rates. Main Conclusions Two traits related to dispersal mobility, range size and fruit colour, were not identified as the main drivers of diversification in palms. Increased model extinction rate complexity led to better performing models, which indicates that net diversification should be estimated rather than speciation alone. However, increased complexity may lead to incorrect SecSSE model conclusions without careful consideration. Finally, we find palms with more mobile dispersers do not have larger range sizes, meaning other factors are more important determinants of range size.

Benson, C. W., M. R. Sheltra, P. J. Maughan, E. N. Jellen, M. D. Robbins, B. S. Bushman, E. L. Patterson, et al. 2023. Homoeologous evolution of the allotetraploid genome of Poa annua L. BMC Genomics 24. https://doi.org/10.1186/s12864-023-09456-5

Background Poa annua (annual bluegrass) is an allotetraploid turfgrass, an agronomically significant weed, and one of the most widely dispersed plant species on earth. Here, we report the chromosome-scale genome assemblies of P. annua’s diploid progenitors, P. infirma and P. supina, and use multi-omic analyses spanning all three species to better understand P. annua’s evolutionary novelty. Results We find that the diploids diverged from their common ancestor 5.5 – 6.3 million years ago and hybridized to form P. annua  ≤ 50,000 years ago. The diploid genomes are similar in chromosome structure and most notably distinguished by the divergent evolutionary histories of their transposable elements, leading to a 1.7 × difference in genome size. In allotetraploid P. annua, we find biased movement of retrotransposons from the larger (A) subgenome to the smaller (B) subgenome. We show that P. annua’s B subgenome is preferentially accumulating genes and that its genes are more highly expressed. Whole-genome resequencing of several additional P. annua accessions revealed large-scale chromosomal rearrangements characterized by extensive TE-downsizing and evidence to support the Genome Balance Hypothesis. Conclusions The divergent evolutions of the diploid progenitors played a central role in conferring onto P. annua its remarkable phenotypic plasticity. We find that plant genes (guided by selection and drift) and transposable elements (mostly guided by host immunity) each respond to polyploidy in unique ways and that P. annua uses whole-genome duplication to purge highly parasitized heterochromatic sequences. The findings and genomic resources presented here will enable the development of homoeolog-specific markers for accelerated weed science and turfgrass breeding .

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.

Wang, Y., J. Wang, T. A. Garran, H. Liu, H. Lin, J. Luo, Q. Yuan, et al. 2023. Genetic diversity and population divergence of Leonurus japonicus and its distribution dynamic changes from the last interglacial to the present in China. BMC Plant Biology 23. https://doi.org/10.1186/s12870-023-04284-x

Background Leonurus japonicus , a significant medicinal plant known for its therapeutic effects on gynecological and cardiovascular diseases, has genetic diversity that forms the basis for germplasm preservation and utilization in medicine. Despite its economic value, limited research has focused on its genetic diversity and divergence. Results The avg. nucleotide diversity of 59 accessions from China were 0.00029 and hotspot regions in petN-psbM and rpl32-trnL (UAG) spacers, which can be used for genotype discrimination. These accessions divided into four clades with significant divergence. The four subclades, which split at approximately 7.36 Ma, were likely influenced by the Hengduan Mountains uplift and global temperature drop. The initial divergence gave rise to Clade D, with a crown age estimated at 4.27 Ma, followed by Clade C, with a crown age estimated at 3.39 Ma. The four clades were not showed a clear spatial distribution. Suitable climatic conditions for the species were identified, including warmest quarter precipitation 433.20 mm ~ 1,524.07 mm, driest month precipitation > 12.06 mm, and coldest month min temp > -4.34 °C. The high suitability distribution showed contraction in LIG to LGM, followed by expansion from LGM to present. The Hengduan Mountains acted as a glacial refuge for the species during climate changes. Conclusions Our findings reflected a clear phylogenetic relationships and divergence within species L. japonicus and the identified hotspot regions could facilitate the genotype discrimination. The divergence time estimation and suitable area simulation revealed evolution dynamics of this species and may propose conservation suggestions and exploitation approaches in the future.

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.