Science Enabled by Specimen Data

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.

Goolsby, J. A., P. J. Moran, M. Martínez Jiménez, C. Yang, K. Canavan, Q. Paynter, N. Ota, and D. J. Kriticos. 2023. Biology of Invasive Plants 4. Arundo donax L. Invasive Plant Science and Management 16: 81–109. https://doi.org/10.1017/inp.2023.17

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.

Jiménez-López, D. A., M. J. Carmona-Higuita, G. Mendieta-Leiva, R. Martínez-Camilo, A. Espejo-Serna, T. Krömer, N. Martínez-Meléndez, and N. Ramírez-Marcial. 2023. Linking different resources to recognize vascular epiphyte richness and distribution in a mountain system in southeastern Mexico. Flora: 152261. https://doi.org/10.1016/j.flora.2023.152261

Mesoamerican mountains are important centers of endemism and diversity of epiphytes. The Sierra Madre of Chiapas in southeastern Mexico is a mountainous region of great ecological interest due to its high biological richness. We present the first checklist of epiphytes for this region based on a compilation of various information sources. In addition, we determined the conservation status for each species based on the Mexican Official Standard (NOM-059-SEMARNAT-2010), endemism based on geopolitical boundaries, spatial completeness with inventory completeness index, richness distribution with range maps, and the relationship between climatic variables (temperature and rainfall) with species richness using generalized additive models. Our dataset includes 9,799 records collected between 1896-2017. Our checklist includes 708 epiphytes within 160 genera and 26 families; the most species-rich family was Orchidaceae (355 species), followed by Bromeliaceae (82) and Polypodiaceae (79). There were 74 species within a category of risk and 59 species considered endemic. Completeness of epiphyte richness suggests that sampling is still largely incomplete, particularly in the lower parts of the mountain system. Species and family range maps show the highest richness at high elevations, while geographically richness increases towards the southeast. Epiphyte richness increases with increased rainfall, although a unimodal pattern was observed along the temperature gradient with a species richness peak between 16-20 C°. The Sierra Madre of Chiapas forms a refuge to more than 40% of all epiphytes reported for Mexico and its existing network of protected areas overlaps with the greatest epiphyte richness.

Ivey, C. T., N. M. Habecker, J. P. Bergmann, J. Ewald, M. E. Frayer, and J. M. Coughlan. 2023. Weak reproductive isolation and extensive gene flow between Mimulus glaucescens and M. guttatus in northern California. Evolution. https://doi.org/10.1093/evolut/qpad044

Abstract Barriers to reproduction are often how progress in speciation is measured. Nonetheless, an unresolved question concerns the extent to which reproductive barriers diminish gene flow between incipient species. The Sierra Nevada foothill endemic Mimulus glaucescens and the widespread M. guttatus are considered distinct species based on striking differences in vegetative morphology, but barriers to reproduction have not been previously identified, nor has gene flow between species been characterized. Here, we examined 15 potential reproductive barriers within a Northern California area of broad sympatry. Most barriers, with the exception of ecogeographic isolation, were weak or absent, and total isolation for each species was incomplete. Population genomic analyses of range-wide and broadly sympatric accessions revealed extensive gene flow between these taxa, particularly in sympatry. Despite widespread introgression, Mimulus glaucescens, emerged as monophyletic and largely comprised a single ancestry that was found at intermediate frequency within M. guttatus. This result, along with observed ecological and phenotypic differentiation, suggests that natural selection may contribute to the maintenance of distinct phenotypic forms in the earliest stages of speciation. Integrating estimates of barrier strength with direct estimates of gene flow can strengthen a more nuanced interpretation of the process of speciation in natural communities.

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.

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.

Lu, L.-L., B.-H. Jiao, F. Qin, G. Xie, K.-Q. Lu, J.-F. Li, B. Sun, et al. 2022. Artemisia pollen dataset for exploring the potential ecological indicators in deep time. Earth System Science Data 14: 3961–3995. https://doi.org/10.5194/essd-14-3961-2022

Abstract. Artemisia, along with Chenopodiaceae, is the dominant component growing in the desert and dry grassland of the Northern Hemisphere. Artemisia pollen with its high productivity, wide distribution, and easy identification is usually regarded as an eco-indicator for assessing aridity and distinguishing grassland from desert vegetation in terms of the pollen relative abundance ratio of Chenopodiaceae/Artemisia (C/A). Nevertheless, divergent opinions on the degree of aridity evaluated by Artemisia pollen have been circulating in the palynological community for a long time. To solve the confusion, we first selected 36 species from nine clades and three outgroups of Artemisia based on the phylogenetic framework, which attempts to cover the maximum range of pollen morphological variation. Then, sampling, experiments, photography, and measurements were taken using standard methods. Here, we present pollen datasets containing 4018 original pollen photographs, 9360 pollen morphological trait measurements, information on 30 858 source plant occurrences, and corresponding environmental factors. Hierarchical cluster analysis on pollen morphological traits was carried out to subdivide Artemisia pollen into three types. When plotting the three pollen types of Artemisia onto the global terrestrial biomes, different pollen types of Artemisia were found to have different habitat ranges. These findings change the traditional concept of Artemisia being restricted to arid and semi-arid environments. The data framework that we designed is open and expandable for new pollen data of Artemisia worldwide. In the future, linking pollen morphology with habitat via these pollen datasets will create additional knowledge that will increase the resolution of the ecological environment in the geological past. The Artemisia pollen datasets are freely available at Zenodo (https://doi.org/10.5281/zenodo.6900308; Lu et al., 2022).

Couvreur, T. L. P., X. Cornejo, J. N. Zapata, and A. Loor. 2022. Two new magnoliid (Annonaceae, Lauraceae) tree species from Manabí, western Ecuador. Blumea - Biodiversity, Evolution and Biogeography of Plants. https://doi.org/10.3767/blumea.2022.67.02.02

Western Ecuador harbours high plant diversity and endemism. The region of Manabí has known intense deforestation over the last decades, but lowland rain forests persist in a network of small forest fragment patches. Here, we describe two new magnoliid tree species from a small privately owned forest fragment known as La Esperanza reserve, in the El Carmen canton (Manabí): Aniba ecuadorica (Lauraceae) and Guatteria esperanzae (Annonaceae). For both species a detailed morphological description, a preliminary conservation status following IUCN criteria, distribution maps and high quality photographs are provided. This represents the second species of Aniba known to occur in western Ecuador, while there are 14 species of Guatteria documented for Ecuador west of the Andes. Aniba ecuadorica is only known from two localities and has a preliminary IUCN conservation status of Critically Endangered, while Guatteria esperanzae is known from six localities and is suggested to be Endangered. Finally, we provide a quick overview of Guatteria species in western Ecuador with a key to the species in the region. The description of these two new tree species underlines the important need of prospection and conservation of the remnant forests in the Manabí region of western Ecuador. We also stress the importance of privately owned forest fragments for biodiversity conservation.

Cano, Á., F. W. Stauffer, T. Andermann, I. M. Liberal, A. Zizka, C. D. Bacon, H. Lorenzi, et al. 2022. Recent and local diversification of Central American understorey palms. Global Ecology and Biogeography 31: 1513–1525. https://doi.org/10.1111/geb.13521

Aim Central America is largely covered by hyperdiverse, yet poorly understood, rain forests. Understorey palms are diverse components of these forests, but little is known about their historical assembly. It is not clear when palms in Central America reached present diversity levels and whether most species arrived from neighbouring regions or evolved locally. We addressed these questions using the most species-rich American palm clades indicative of rain forests. We reconstructed and compared their phylogenomic and biogeographical history with the diversification of 54 other plant lineages, to gain a better understanding of the processes that shaped the assembly of Central American rain forests. Location Central America. Time period Cretaceous to present. Major taxa studied Arecaceae: Arecoideae: Bactridinae, Chamaedoreeae, Geonomateae. Methods We sampled 218 species through fieldwork and living collections. We sequenced their genomic DNA using target sequence-capture procedures. Using 12 calibration points, we reconstructed dated phylogenies under three approaches (multispecies coalescent, maximum likelihood and Bayesian inference), conducted biogeographical analyses (dispersal–extinction–cladogenesis) and estimated phylogenetic diversity metrics. Results Dated phylogenies revealed intense diversification in Central America from 12 Ma. Local diversification events were four times more frequent than dispersal events, and we found strong phylogenetic clustering in relationship to Central America. Main conclusions Our results suggest that most understorey palm species that characterize the Central American rain forests today evolved locally after repeated dispersal events, mostly from South America. Understorey palms in Central American rain forests diversified primarily after closure of the Central American Seaway at c. 13 Ma, suggesting that the Great American Biotic Interchange was a major trigger for plant diversification in Central American rain forests. This recent diversification contrasts with the much earlier existence of rain forest palms in neighbouring South America since c. 58 Ma. We found similar timings of diversification in 54 other seed plant lineages, suggesting an unexpectedly recent assembly of the hyperdiverse Central American flora.