Science Enabled by Specimen Data

Campbell, L. C. E., E. T. Kiers, and G. Chomicki. 2022. The evolution of plant cultivation by ants. Trends in Plant Science. https://doi.org/10.1016/j.tplants.2022.09.005

Outside humans, true agriculture was previously thought to be restricted to social insects farming fungus. However, obligate farming of plants by ants was recently discovered in Fiji, prompting a re-examination of plant cultivation by ants. Here, we generate a database of plant cultivation by ants, identify three main types, and show that these interactions evolved primarily for shelter rather than food. We find that plant cultivation evolved at least 65 times independently for crops (~200 plant species), and 15 times in farmer lineages (~37 ant taxa) in the Neotropics and Asia/Australasia. Because of their high evolutionary replication, and variation in partner dependence, these systems are powerful models to unveil the steps in the evolution and ecology of insect agriculture.

Testo, W. L., A. L. de Gasper, S. Molino, J. M. G. y Galán, A. Salino, V. A. de O. Dittrich, and E. B. Sessa. 2022. Deep vicariance and frequent transoceanic dispersal shape the evolutionary history of a globally distributed fern family. American Journal of Botany. https://doi.org/10.1002/ajb2.16062

Premise Historical biogeography of ferns is typically expected to be dominated by long-distance dispersal, due to their minuscule spores. However, few studies have inferred the historical biogeography of a large and widely distributed group of ferns to test this hypothesis. Our aims are to determine the extent to which long-distance dispersal vs. vicariance have shaped the history of the fern family Blechnaceae, to explore ecological correlates of dispersal and diversification, and to determine whether these patterns differ between the northern and southern hemispheres. Methods We used sequence data for three chloroplast loci to infer a time-calibrated phylogeny for 154 out of 265 species of Blechnaceae, including representatives of all genera in the family. This tree was used to conduct ancestral range reconstruction and stochastic character mapping, estimate diversification rates, and identify ecological correlates of diversification. Key results Blechnaceae originated in Eurasia and began diversifying in the late Cretaceous. A lineage comprising most extant diversity diversified principally in the austral Pacific region around the Paleocene-Eocene Thermal Maximum. Land connections that existed near the poles during periods of warm climates likely facilitated migration of several lineages, with subsequent climate-mediated vicariance shaping current distributions. Long-distance dispersal is frequent and asymmetrical, with New Zealand/Pacific Islands, Australia, and tropical America being major source areas. Conclusions Ancient vicariance and extensive long-distance dispersal have shaped the history of Blechnaceae in both the northern and southern hemispheres. The exceptional diversity in austral regions appears to reflect rapid speciation in these areas; mechanisms underlying this evolutionary success remain uncertain.

Amaral, D. T., I. A. S. Bonatelli, M. Romeiro-Brito, E. M. Moraes, and F. F. Franco. 2022. Spatial patterns of evolutionary diversity in Cactaceae show low ecological representation within protected areas. Biological Conservation 273: 109677. https://doi.org/10.1016/j.biocon.2022.109677

Mapping biodiversity patterns across taxa and environments is crucial to address the evolutionary and ecological dimensions of species distribution, suggesting areas of particular importance for conservation purposes. Within Cactaceae, spatial diversity patterns are poorly explored, as are the abiotic factors that may predict these patterns. We gathered geographic and genetic data from 921 cactus species by exploring both the occurrence and genetic databases, which are tightly associated with drylands, to evaluate diversity patterns, such as phylogenetic diversity and endemism, paleo-, neo-, and superendemism, and the environmental predictor variables of such patterns in a global analysis. Hotspot areas of cacti diversity are scattered along the Neotropical and Nearctic regions, mainly in the desertic portion of Mesoamerica, Caribbean Island, and the dry diagonal of South America. The geomorphological features of these regions may create a complexity of areas that work as locally buffered zones over time, which triggers local events of diversification and speciation. Desert and dryland/dry forest areas comprise paleo- and superendemism and may act as both museums and cradles of species, displaying great importance for conservation. Past climates, topography, soil features, and solar irradiance seem to be the main predictors of distinct endemism types. The hotspot areas that encompass a major part of the endemism cells are outside or poorly covered by formal protection units. The current legally protected areas are not able to conserve the evolutionary diversity of cacti. Given the rapid anthropogenic disturbance, efforts must be reinforced to monitor biodiversity and the environment and to define/plan current and new protected areas.

Sánchez, C. A., H. Li, K. L. Phelps, C. Zambrana-Torrelio, L.-F. Wang, P. Zhou, Z.-L. Shi, et al. 2022. A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia. Nature Communications 13. https://doi.org/10.1038/s41467-022-31860-w

Emerging diseases caused by coronaviruses of likely bat origin (e.g., SARS, MERS, SADS, COVID-19) have disrupted global health and economies for two decades. Evidence suggests that some bat SARS-related coronaviruses (SARSr-CoVs) could infect people directly, and that their spillover is more frequent than previously recognized. Each zoonotic spillover of a novel virus represents an opportunity for evolutionary adaptation and further spread; therefore, quantifying the extent of this spillover may help target prevention programs. We derive current range distributions for known bat SARSr-CoV hosts and quantify their overlap with human populations. We then use probabilistic risk assessment and data on human-bat contact, human viral seroprevalence, and antibody duration to estimate that a median of 66,280 people (95% CI: 65,351–67,131) are infected with SARSr-CoVs annually in Southeast Asia. These data on the geography and scale of spillover can be used to target surveillance and prevention programs for potential future bat-CoV emergence. Coronaviruses may spill over from bats to humans. This study uses epidemiological data, species distribution models, and probabilistic risk assessment to map overlap among people and SARSr-CoV bat hosts and estimate how many people are infected with bat-origin SARSr-CoVs in Southeast Asia annually.

Sáenz-Ceja, J. E., J. T. Sáenz-Reyes, and D. Castillo-Quiroz. 2022. Pollinator Species at Risk from the Expansion of Avocado Monoculture in Central Mexico. Conservation 2: 457–472. https://doi.org/10.3390/conservation2030031

The monoculture of avocado (Persea americana) has triggered the loss of large forested areas in central Mexico, including the habitat of threatened species. This study assessed the potential habitat loss of ten threatened pollinator species due to the expansion of avocado monoculture in Mexico. First, we modeled the distribution of avocado and pollinators. Then, we overlapped their suitable areas at a national level and within the Trans-Mexican Volcanic Belt (TMVB). We also identified the areas with more affected pollinators and coinciding with protected areas. As a result, 78% of the suitable areas for avocado coincided with the distribution of at least one pollinator. Although only two pollinators lost more than one-fifth of their distribution at a national level, the habitat loss increased to 41.6% on average, considering their distribution within the TMVB. The most affected pollinators were Bombus brachycephalus, B diligens, Danaus plexippus, and Tilmatura dupontii, losing more than 48% of their distribution within this ecoregion. The areas with a greater number of affected species pollinators were found in the states of Michoacán, Mexico, and Morelos, where most of the area is currently unprotected. Our results suggest that the expansion of the avocado monoculture will negatively affect the habitat of threatened pollinators in Mexico.

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.

Williams, C. J. R., D. J. Lunt, U. Salzmann, T. Reichgelt, G. N. Inglis, D. R. Greenwood, W. Chan, et al. 2022. African Hydroclimate During the Early Eocene From the DeepMIP Simulations. Paleoceanography and Paleoclimatology 37. https://doi.org/10.1029/2022pa004419

The early Eocene (∼56‐48 million years ago) is characterised by high CO2 estimates (1200‐2500 ppmv) and elevated global temperatures (∼10 to 16°C higher than modern). However, the response of the hydrological cycle during the early Eocene is poorly constrained, especially in regions with sparse data coverage (e.g. Africa). Here we present a study of African hydroclimate during the early Eocene, as simulated by an ensemble of state‐of‐the‐art climate models in the Deep‐time Model Intercomparison Project (DeepMIP). A comparison between the DeepMIP pre‐industrial simulations and modern observations suggests that model biases are model‐ and geographically dependent, however these biases are reduced in the model ensemble mean. A comparison between the Eocene simulations and the pre‐industrial suggests that there is no obvious wetting or drying trend as the CO2 increases. The results suggest that changes to the land sea mask (relative to modern) in the models may be responsible for the simulated increases in precipitation to the north of Eocene Africa. There is an increase in precipitation over equatorial and West Africa and associated drying over northern Africa as CO2 rises. There are also important dynamical changes, with evidence that anticyclonic low‐level circulation is replaced by increased south‐westerly flow at high CO2 levels. Lastly, a model‐data comparison using newly‐compiled quantitative climate estimates from palaeobotanical proxy data suggests a marginally better fit with the reconstructions at lower levels of CO2.

Reichgelt, T., D. R. Greenwood, S. Steinig, J. G. Conran, D. K. Hutchinson, D. J. Lunt, L. J. Scriven, and J. Zhu. 2022. Plant Proxy Evidence for High Rainfall and Productivity in the Eocene of Australia. Paleoceanography and Paleoclimatology 37. https://doi.org/10.1029/2022pa004418

During the early to middle Eocene, a mid‐to‐high latitudinal position and enhanced hydrological cycle in Australia would have contributed to a wetter and “greener” Australian continent where today arid to semi‐arid climates dominate. Here, we revisit 12 southern Australian plant megafossil sites from the early to middle Eocene to generate temperature, precipitation and seasonality paleoclimate estimates, net primary productivity (NPP) and vegetation type, based on paleobotanical proxies and compare to early Eocene global climate models. Temperature reconstructions are uniformly subtropical (mean annual, summer, and winter mean temperatures 19–21 °C, 25–27 °C and 14–16 °C, respectively), indicating that southern Australia was ∼5 °C warmer than today, despite a >20° poleward shift from its modern geographic location. Precipitation was less homogeneous than temperature, with mean annual precipitation of ∼60 cm over inland sites and >100 cm over coastal sites. Precipitation may have been seasonal with the driest month receiving 2–7× less than mean monthly precipitation. Proxy‐model comparison is favorable with an 1680 ppm CO2 concentration. However, individual proxy reconstructions can disagree with models as well as with each other. In particular, seasonality reconstructions have systemic offsets. NPP estimates were higher than modern, implying a more homogenously “green” southern Australia in the early to middle Eocene, when this part of Australia was at 48–64 °S, and larger carbon fluxes to and from the Australian biosphere. The most similar modern vegetation type is modern‐day eastern Australian subtropical forest, although distance from coast and latitude may have led to vegetation heterogeneity.

Colli-Silva, M., J. R. Pirani, and A. Zizka. 2022. Ecological niche models and point distribution data reveal a differential coverage of the cacao relatives (Malvaceae) in South American protected areas. Ecological Informatics 69: 101668. https://doi.org/10.1016/j.ecoinf.2022.101668

For many regions, such as in South America, it is unclear how well the existent protected areas network (PAs) covers different taxonomic groups and if there is a coverage bias of PAs towards certain biomes or species. Publicly available occurrence data along with ecological niche models might help to overcome this gap and to quantify the coverage of taxa by PAs ensuring an unbiased distribution of conservation effort. Here, we use an occurrence database of 271 species from the cacao family (Malvaceae) to address how South American PAs cover species with different distribution, abundance, and threat status. Furthermore, we compared the performance of online databases, expert knowledge, and modelled species distributions in estimating species coverage in PAs. We found 79 species from our survey (29% of the total) lack any record inside South American PAs and that 20 out of 23 species potentially threatened with extinction are not covered by PAs. The area covered by South American PAs was low across biomes, except for Amazonia, which had a relative high PA coverage, but little information on species distribution within PA available. Also, raw geo-referenced occurrence data were underestimating the number of species in PAs, and projections from ecological niche models were more prone to overestimating the number of species represented within PAs. We discuss that the protection of South American flora in heterogeneous environments demand for specific strategies tailored to particular biomes, including making new collections inside PAs in less collected areas, and the delimitation of more areas for protection in more known areas. Also, by presenting biasing scenarios of collection effort in a representative plant group, our results can benefit policy makers in conserving different spots of tropical environments highly biodiverse.

Sluiter, I. R. K., G. R. Holdgate, T. Reichgelt, D. R. Greenwood, A. P. Kershaw, and N. L. Schultz. 2022. A new perspective on Late Eocene and Oligocene vegetation and paleoclimates of South-eastern Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 596: 110985. https://doi.org/10.1016/j.palaeo.2022.110985

We present a composite terrestrial pollen record of latest Eocene through Oligocene (35.5–23 Ma) vegetation and climate change from the Gippsland Basin of south-eastern Australia. Climates were overwhelmingly mesothermic through this time period, with mean annual temperature (MAT) varying between 13 and 18 °C, with an average of 16 °C. We provide evidence to support a cooling trend through the Eocene–Oligocene Transition (EOT), but also identify three subsequent warming cycles through the Oligocene, leading to more seasonal climates at the termination of the Epoch. One of the warming episodes in the Early Oligocene appears to have also occurred at two other southern hemisphere sites at the Drake Passage as well as off eastern Tasmania, based on recent research. Similarities with sea surface temperature records from modern high southern latitudes which also record similar cycles of warming and cooling, are presented and discussed. Annual precipitation varied between 1200 and 1700 mm/yr, with an average of 1470 mm/yr through the sequence. Notwithstanding the extinction of Nothofagus sg. Brassospora from Australia and some now microthermic humid restricted Podocarpaceae conifer taxa, the rainforest vegetation of lowland south-eastern Australia is reconstructed to have been similar to present day Australian Evergreen Notophyll Vine Forests existing under the sub-tropical Köppen-Geiger climate class Cfa (humid subtropical) for most of the sequence. Short periods of cooler climates, such as occurred through the EOT when MAT was ~ 13 °C, may have supported vegetation similar to modern day Evergreen Microphyll Fern Forest. Of potentially greater significance, however, was a warm period in the Early to early Late Oligocene (32–26 Ma) when MAT was 17–18 °C, accompanied by small but important increases in Araucariaceae pollen. At this time, Araucarian Notophyll/Microphyll Vine Forest likely occurred regionally.