Science Enabled by Specimen Data

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.

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.

Issaly, E. A., M. C. Baranzelli, N. Rocamundi, A. M. Ferreiro, L. A. Johnson, A. N. Sérsic, and V. Paiaro. 2023. Too much water under the bridge: unraveling the worldwide invasion of the tree tobacco through genetic and ecological approaches. Biological Invasions. https://doi.org/10.1007/s10530-023-03189-y

Understanding how, and from where, invasive species were introduced is critical for revealing the invasive mechanism, explaining the invasion success, and providing crucial insights for effective management. Here, we combined a phylogeographic approach with ecological niche modeling comparisons to elucidate the introduction mode and source of Nicotiana glauca , a native South American species that is now invasive worldwide. We tested three different scenarios based on the invasion source—random native, restricted native, and bridgehead invasive—considering genetic diversity and climatic niche comparisons among native and invaded areas. We found three genetic lineages geographically and climatically differentiated within the native range. Only one of these genetic groups contained the invasive haplotypes, but showed no climatic niche overlap with any invaded area. Conversely, one invaded area located in western South America, with more genetic diversity than other invaded areas but less than the native range, showed climatic niche overlap with almost all other invaded areas worldwide. These findings indicate that N. glauca first likely invaded the southernmost areas beyond its native range, forming a bridgehead invasive source, from which the species subsequently invaded other regions around the world. Invasiveness would have been fostered by changes in the environmental preferences of the species in the bridgehead area, towards drier, colder and less seasonal climates, becoming the actual source of invasion to areas climatically similar throughout the world. The fine scale resolution analyses combining genetic and climatic approaches within the native range were essential to illuminating the introduction scenario of this invasive species.

Barrett, C. F., C. W. Corbett, and H. L. Thixton-Nolan. 2023. A lack of population structure characterizes the invasive Lonicera japonica in West Virginia and across eastern North America1,2. The Journal of the Torrey Botanical Society 150. https://doi.org/10.3159/torrey-d-23-00007.1

Invasive plant species cause massive ecosystem damage globally yet represent powerful case studies in population genetics and rapid adaptation to new habitats. The availability of digitized herbarium collections data, and the ubiquity of invasive species across the landscape make them highly accessible for studies of invasion history and population dynamics associated with their introduction, establishment, spread, and ecological interactions. Here we focus on Lonicera japonica, one of the most damaging invasive vine species in North America. We leveraged digitized collections data and contemporary field collections to reconstruct the invasion history and characterize patterns of genomic variation in the eastern USA, using a straightforward method for generating nucleotide polymorphism data and a recently published, chromosome-level genome for the species. We found an overall lack of population structure among sites in northern West Virginia, USA, as well as across sites in the central and eastern USA. Heterozygosity and population differentiation were both low based on FST analysis of molecular variance, principal components analysis, and cluster-based analyses. We also found evidence of high inbreeding coefficients and significant linkage disequilibrium, in line with the ability of this otherwise outcrossing, perennial species to propagate vegetatively. Our findings corroborate earlier studies based on allozyme data, and suggest that intentional, human-assisted spread explains the lack of population structure, as this species was planted for erosion control and as an ornamental, escaping cultivation repeatedly across the USA.

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.

Freire-Fierro, A., F. Forest, D. S. Devey, J. F. B. Pastore, J. W. Horn, X.-J. Ge, Z. Wang, et al. 2023. Monnina (Polygalaceae), a New World monophyletic genus full of contrasts. Botanical Journal of the Linnean Society. https://doi.org/10.1093/botlinnean/boad026

Endemic to the Neotropics, Monnina is the second largest genus of Polygalaceae, yet little is known about its phylogenetic history, biogeography, and morphological character evolution. To address these knowledge gaps, we conducted Bayesian and maximum likelihood (ML) analyses of nuclear ITS and plastid trnL–F regions to test the monophyly of Monnina s.l. We used this phylogenetic framework to (i) infer divergence time estimates of lineages within the genus and reconstruct their historical biogeography; (ii) reconstruct the evolution of morphological characters of putative ecological and evolutionary importance in Monnina; and (iii) test for correlations between our phylogenetic hypothesis and environmental data. Our results reveal that Monnina is monophyletic with an indehiscent, 1–2-seeded fruit as a synapomorphy for the genus. We identify six clades within Monnina based on our combined phylogenetic results: Clades A, B, and D are primarily distributed in southern and eastern South America, Clades C and E are primarily Central Andean, and Clade F is chiefly distributed in the Northern Andes and Central America. The ancestor of the Monnina stem lineage dispersed from Australia/Africa to South America during the late Eocene to early Oligocene. The divergences of major lineages within the genus began in the early Miocene. We inferred the most recent common ancestor of Monnina to be an herbaceous plant with one-seeded samaroid fruits. The origins of fleshy fruits and shrubby habits are phylogenetically correlated within Monnina, and their concerted convergent evolution may have promoted increased net diversification rates in the two most species-rich subclades of the genus.

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.

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.

Geier, C., J. M. Bouchal, S. Ulrich, D. Uhl, T. Wappler, S. Wedmann, R. Zetter, et al. 2023. Potential pollinators and paleoecological aspects of Eocene Ludwigia (Onagraceae) from Eckfeld, Germany. Palaeoworld. https://doi.org/10.1016/j.palwor.2023.07.003

Paleogene flower-insect interactions and paleo-pollination processes are, in general, poorly understood and fossil evidence for such floral and faunal interactions are rarely reported. To shed light on angiosperm flower-insect interactions, we investigated several hundred fossil flowers and insects from the middle Eocene Fossil Lagerstätte of Eckfeld, Germany. During our work, we discovered a unique fossil Ludwigia flower (bud) with in situ pollen. The ecological preferences (climate, biome, habitat, etc.) of extant Ludwigia and the paleoecological configurations of the fossil plant assemblage support the taxonomic affiliation of the flower bud and an Eocene presence of Ludwigia in the vicinity of the former Lake Eckfeld. Today’s Ludwigia are mostly pollinated by Hymenoptera (bees). Therefore, we screened all currently known hymenopteran fossils from Eckfeld but found no Ludwigia pollen adhering to any of the specimens. On the contrary, we discovered Ludwigia pollen adhering to two different groups of Coleoptera (beetles). Our study suggests that during the Eocene of Europe, Ludwigia flowers were visited and probably pollinated by beetles and over time there was a shift in primary flower visitors/pollinators, from beetles to bees, sometime during the late Paleogene to Neogene.