Evolutionary history of host trees amplifies the dilution effect of biodiversity on forest pests.

Biodiversity appears to strongly suppress pathogens and pests in many plant and animal systems. However, this "dilution effect" is not consistently detected, and when present can vary strikingly in magnitude. Here, we use forest inventory data from over 25,000 plots (>1.1 million sampled trees) to quantify the strength of the dilution effect on dozens of forest pests and clarify why some pests are particularly sensitive to biodiversity. Using Bayesian hierarchical models, we show that pest prevalence is frequently lower in highly diverse forests, but there is considerable variability in the magnitude of this dilution effect among pests. The strength of dilution was not closely associated with host specialization or pest nativity. Instead, pest prevalence was lower in forests where co-occurring tree species were more distantly related to a pest's preferred hosts. Our analyses indicate that host evolutionary history and forest composition are key to understanding how species diversity may dilute the impacts of tree pests, with important implications for predicting how future biodiversity change may affect the spread and distribution of damaging forest pests.

A global analysis of tree pests and emerging pest threats.

SignificanceThe introduction of trees outside their native ranges has greatly expanded the potential ranges of their pathogens and insect pests, which risk spilling over and impacting native flora. However, we often lack a strong understanding of the host, climatic, and geographic factors that allow pests to establish outside their hosts' native ranges. Using global datasets of pest occurrences and the native and nonnative ranges of tree hosts, we show there are strong generalizable trends controlling pest occurrences and can predict the occurrence of pests outside their hosts' native ranges with >75% accuracy. Our modeling framework offers a powerful tool to identify future invasive pest species and the ecological mechanisms controlling the accumulation of pests outside their hosts' native ranges.

Combining camera trap surveys and IUCN range maps to improve knowledge of species distributions.

Reliable maps of species distributions are fundamental for biodiversity research and conservation. The International Union for Conservation of Nature (IUCN) range maps are widely recognized as authoritative representations of species' geographic limits, yet they might not always align with actual occurrence data. In recent area of habitat (AOH) maps, areas that are not habitat have been removed from IUCN ranges to reduce commission errors, but their concordance with actual species occurrence also remains untested. We tested concordance between occurrences recorded in camera trap surveys and predicted occurrences from the IUCN and AOH maps for 510 medium- to large-bodied mammalian species in 80 camera trap sampling areas. Across all areas, cameras detected only 39% of species expected to occur based on IUCN ranges and AOH maps; 85% of the IUCN only mismatches occurred within 200 km of range edges. Only 4% of species occurrences were detected by cameras outside IUCN ranges. The probability of mismatches between cameras and the IUCN range was significantly higher for smaller-bodied mammals and habitat specialists in the Neotropics and Indomalaya and in areas with shorter canopy forests. Our findings suggest that range and AOH maps rarely underrepresent areas where species occur, but they may more often overrepresent ranges by including areas where a species may be absent, particularly at range edges. We suggest that combining range maps with data from ground-based biodiversity sensors, such as camera traps, provides a richer knowledge base for conservation mapping and planning.

Combinación de censos con fototrampas y mapas de extensión de la UICN para incrementar el conocimiento sobre la distribución de las especies Resumen Los mapas confiables de la distribución de las especies son fundamentales para la investigación y conservación de la biodiversidad. Los mapas de distribución de la Unión Internacional para la Conservación de la Naturaleza (UICN) están reconocidos como representaciones de autoridad de los límites geográficos de las especies, aunque no siempre se alinean con los datos actuales de su presencia. En los mapas recientes de área de hábitat (ADH), las áreas que no son hábitat han sido eliminadas de la distribución de la UICN para reducir los errores de comisión, pero su concordancia con la presencia actual de las especies tampoco ha sido analizada. Analizamos la concordancia entre la presencia registrada por los censos de fototrampas y pronosticamos la presencia a partir de los mapas de la UICN y de ADH de 510 especies de mamíferos de talla mediana a grande en 80 áreas de muestreo de fototrampas. Las cámaras detectaron sólo el 39% de las especies esperadas con base en la distribución de la UICN y los mapas de ADH en todas las áreas; el 85% de las disparidades con la UICN ocurrieron dentro de los 200 km a partir del borde de la distribución. Sólo el 4% de la presencia de las especies fue detectada por las cámaras ubicadas fuera de la distribución de la UICN. La probabilidad de disparidad entre las cámaras y la UICN fue significativamente mayor para los mamíferos de talla pequeña y para los especialistas de hábitat en las regiones Neotropical e Indomalaya y en áreas con doseles forestales más bajos. Nuestros hallazgos sugieren que los mapas de distribución y ADH pocas veces subrepresentan las áreas con presencia de las especies, pero con frecuencia pueden sobrerrepresentar la distribución al incluir áreas en donde las especies pueden estar ausentes, en particular los bordes de la distribución. Sugerimos que la combinación de los mapas de distribución con los sensores de biodiversidad en tierra, como las fototrampas, proporciona una base más rica de conocimiento para el mapeo y la planeación de la conservación.

Host phylogenetic diversity predicts the global extent and composition of tree pests.

Tree pests cause billions of dollars of damage annually; yet, we know little about what limits their regional composition and distribution. Here, we model the co-occurrence of 4510 pests and 981 tree host genera spread across 233 countries. We show the composition of tree pests is primarily driven by the phylogenetic composition of host trees, whereas effects of climate and geography tend to be more minor. Pests that utilise many hosts tend to be more widespread; however, most pests do not fill the geographic range of their hosts-indicating that many pests could expand their extents if able to overcome barriers limiting their current distribution. Our results suggest that the establishment of pests in new regions may be largely dictated by the presence of suitable host trees, but more work is needed to fully understand the influences climate has on the distributions of individual pest species.

Phylogenetic and functional clustering illustrate the roles of adaptive radiation and dispersal filtering in jointly shaping late-Quaternary mammal assemblages on oceanic islands.

Islands frequently harbour unique assemblages of species, yet their ecological roles and differences are largely ignored in island biogeography studies. Here, we examine eco-evolutionary processes structuring mammal assemblages on oceanic islands worldwide, including all extant and extinct late-Quaternary mammal species. We find island mammal assemblages tend to be phylogenetically clustered (share more recent evolutionary histories), with clustering increasing with island area and isolation. We also observe that mammal assemblages often tend to be functionally clustered (share similar traits), but the strength of clustering is weak and generally independent from island area or isolation. These findings indicate the important roles of in situ speciation and dispersal filtering in shaping island mammal assemblages under pre-anthropogenic conditions, notably through adaptive radiation of a few clades (e.g. bats, with generally high dispersal abilities). Our study demonstrates that considering the functional and phylogenetic axes of diversity can better reveal the eco-evolutionary processes of island community assembly.

Predicting missing links in global host-parasite networks.

1. Parasites that infect multiple species cause major health burdens globally, but for many, the full suite of susceptible hosts is unknown. Predicting undocumented host-parasite associations will help expand knowledge of parasite host specificities, promote the development of theory in disease ecology and evolution, and support surveillance of multi-host infectious diseases. The analysis of global species interaction networks allows for leveraging of information across taxa, but link prediction at this scale is often limited by extreme network sparsity and lack of comparable trait data across species. 2. Here we use recently developed methods to predict missing links in global mammal-parasite networks using readily available data: network properties and evolutionary relationships among hosts. We demonstrate how these link predictions can efficiently guide the collection of species interaction data and increase the completeness of global species interaction networks. 3. We amalgamate a global mammal host-parasite interaction network (>29,000 interactions) and apply a hierarchical Bayesian approach for link prediction that leverages information on network structure and scaled phylogenetic distances among hosts. We use these predictions to guide targeted literature searches of the most likely yet undocumented interactions, and identify empirical evidence supporting many of the top 'missing' links. 4. We find that link prediction in global host-parasite networks can successfully predict parasites of humans, domesticated animals and endangered wildlife, representing a combination of published interactions missing from existing global databases, and potential but currently undocumented associations. 5. Our study provides further insight into the use of phylogenies for predicting host-parasite interactions, and highlights the utility of iterated prediction and targeted search to efficiently guide the collection of information on host-parasite interactions. These data are critical for understanding the evolution of host specificity, and may be used to support disease surveillance through a process of predicting missing links, and targeting research towards the most likely undocumented interactions.

Disease mortality in domesticated animals is predicted by host evolutionary relationships.

Infectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multihost parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multihost parasites. Here, using a global dataset of >4,000 case-fatality rates for 65 infectious diseases (caused by microparasites and macroparasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phylogenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts.

Ecophylogenetics redux.

Species' evolutionary histories shape their present-day ecologies, but the integration of phylogenetic approaches in ecology has had a contentious history. The field of ecophylogenetics promised to reveal the process of community assembly from simple indices of phylogenetic pairwise distances - communities shaped by environmental filtering were composed of closely related species, whereas communities shaped by competition were composed of less closely related species. However, the mapping of ecology onto phylogeny proved to be not so straightforward, and the field remains mired in controversy. Nonetheless, ecophylogenetic methods provided important advances across ecology. For example the phylogenetic distances between species is a strong predictor of pest and pathogen sharing, and can thus inform models of species invasion, coexistence and the disease dilution/amplification effect of biodiversity. The phylogenetic structure of communities may also provide information on niche space occupancy, helping interpret patterns of facilitation, succession and ecosystem functioning - with relevance for conservation and restoration - and the dynamics among species within foodwebs and metacommunities. I suggest leveraging advances in our understanding of the process of evolution on phylogenetic trees would allow the field to progress further, while maintaining the essence of the original vision that proved so seductive.

Opposing macroevolutionary and trait-mediated patterns of threat and naturalisation in flowering plants.

Due to expanding global trade and movement of people, new plant species are establishing in exotic ranges at increasing rates while the number of native species facing extinction from multiple threats grows. Yet, how species losses and gains globally may, together, be linked to traits and macroevolutionary processes is poorly understood. Here, we show that, adjusting for diversification rate and clade age, the proportion of threatened species across flowering plant families is negatively related to the proportion of naturalised species per family. Moreover, naturalisation is positively associated with range size, short generation time, autonomous seed production and interspecific hybridisation, but negatively with age and diversification, whereas threat is negatively associated with range size and hybridisation, and positively with biotic pollination, age and diversification rate. That we find such a pronounced signature of naturalisation and threat across plant families suggests that both trait syndromes have coexisted over deep evolutionary time and counter to intuition, that neither strategy is necessarily superior to the other over long evolutionary timespans.

Phenological sensitivity to temperature mediates herbivory.

Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature-sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature-sensitive, co-occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously underappreciated cost to phenological tracking of climate change over longer timescales.

The macroecology and macroevolution of plant species at risk.

Contents Summary 708 I. Introduction 708 II. Fossils and phylogenies: learning from our past 708 III. Threatened species and Red Lists 710 IV. The geography of threat 710 V. The taxonomy of threat 710 VI. Predicting species at risk 711 VII. Conclusion 711 Acknowledgements 712 References 712 SUMMARY: Current rates of extinction are unprecedented in human history. The fossil record and newer molecular phylogenies illuminate historical patterns of speciation and extinction. They reveal both spectacular radiations and the characteristic features of mass extinction events in our geological past. The IUCN Red List provides insight into present-day species declines. There is emerging synthesis that species at risk are nonrandomly distributed across space and phylogeny. This pattern may be explained by geographical variation in driver intensity and species differential sensitivities. However, traits that confer resistance to one global change driver may increase susceptibility to a different driver. A complete understanding of extinction risk requires consideration of the interaction between extinction drivers, ecological traits, and species' evolutionary histories.

Bacterial diversity in the waterholes of the Kruger National Park: an eDNA metabarcoding approach 1.

Bacteria are essential components of natural environments. They contribute to ecosystem functioning through roles as mutualists and pathogens for larger species, and as key components of food webs and nutrient cycles. Bacterial communities respond to environmental disturbances, and the tracking of these communities across space and time may serve as indicators of ecosystem health in areas of conservation concern. Recent advances in DNA sequencing of environmental samples allow for rapid and culture-free characterization of bacterial communities. Here we conduct the first metabarcoding survey of bacterial diversity in the waterholes of the Kruger National Park, South Africa. We show that eDNA can be amplified from waterholes and find strongly structured microbial communities, likely reflecting local abiotic conditions, animal ecology, and anthropogenic disturbance. Over timescales from days to weeks we find increased turnover in community composition, indicating bacteria may represent host-associated taxa of large vertebrates visiting the waterholes. Through taxonomic annotation we also identify pathogenic taxa, demonstrating the utility of eDNA metabarcoding for surveillance of infectious diseases. These samples serve as a baseline survey of bacterial diversity in the Kruger National Park, and in the future, spatially distinct microbial communities may be used as markers of ecosystem disturbance, or biotic homogenization across the park.

Spiny plants, mammal browsers, and the origin of African savannas.

Savannas first began to spread across Africa during the Miocene. A major hypothesis for explaining this vegetation change is the increase in C4 grasses, promoting fire. We investigated whether mammals could also have contributed to savanna expansion by using spinescence as a marker of mammal herbivory. Looking at the present distribution of 1,852 tree species, we established that spinescence is mainly associated with two functional types of mammals: large browsers and medium-sized mixed feeders. Using a dated phylogeny for the same tree species, we found that spinescence evolved at least 55 times. The diversification of spiny plants occurred long after the evolution of Afrotherian proboscideans and hyracoids. However, it is remarkably congruent with diversification of bovids, the lineage including the antelope that predominantly browse these plants today. Our findings suggest that herbivore-adapted savannas evolved several million years before fire-maintained savannas and probably, in different environmental conditions. Spiny savannas with abundant mammal herbivores occur in drier climates and on nutrient-rich soils, whereas fire-maintained savannas occur in wetter climates on nutrient-poor soils.

On the relationship between phylogenetic diversity and trait diversity.

Niche differences are key to understanding the distribution and structure of biodiversity. To examine niche differences, we must first characterize how species occupy niche space, and two approaches are commonly used in the ecological literature. The first uses species traits to estimate multivariate trait space (so-called functional trait diversity, FD); the second quantifies the amount of time or evolutionary history captured by a group of species (phylogenetic diversity, PD). It is often-but controversially-assumed that these putative measures of niche space are at a minimum correlated and perhaps redundant, since more evolutionary time allows for greater accumulation of trait changes. This theoretical expectation remains surprisingly poorly evaluated, particularly in the context of multivariate measures of trait diversity. We evaluated the relationship between phylogenetic diversity and trait diversity using analytical and simulation-based methods across common models of trait evolution. We show that PD correlates with FD increasingly strongly as more traits are included in the FD measure. Our results indicate that phylogenetic diversity can be a useful surrogate for high-dimensional trait diversity, but we also show that the correlation weakens when the underlying process of trait evolution includes variation in rate and optima.

Habitat filtering not dispersal limitation shapes oceanic island floras: species assembly of the Galápagos archipelago.

Remote locations, such as oceanic islands, typically harbour relatively few species, some of which go on to generate endemic radiations. Species colonising these locations tend to be a non-random subset from source communities, which is thought to reflect dispersal limitation. However, non-random colonisation could also result from habitat filtering, whereby only a few continental species can become established. We evaluate the imprints of these processes on the Galápagos flora by analysing a comprehensive regional phylogeny for ~ 39 000 species alongside information on dispersal strategies and climatic suitability. We found that habitat filtering was more important than dispersal limitation in determining species composition. This finding may help explain why adaptive radiation is common on oceanic archipelagoes - because colonising species can be relatively poor dispersers with specific niche requirements. We suggest that the standard assumption that plant communities in remote locations are primarily shaped by dispersal limitation deserves reconsideration.

Improving phylogenetic regression under complex evolutionary models.

Phylogenetic Generalized Least Square (PGLS) is the tool of choice among phylogenetic comparative methods to measure the correlation between species features such as morphological and life-history traits or niche characteristics. In its usual form, it assumes that the residual variation follows a homogenous model of evolution across the branches of the phylogenetic tree. Since a homogenous model of evolution is unlikely to be realistic in nature, we explored the robustness of the phylogenetic regression when this assumption is violated. We did so by simulating a set of traits under various heterogeneous models of evolution, and evaluating the statistical performance (type I error [the percentage of tests based on samples that incorrectly rejected a true null hypothesis] and power [the percentage of tests that correctly rejected a false null hypothesis]) of classical phylogenetic regression. We found that PGLS has good power but unacceptable type I error rates. This finding is important since this method has been increasingly used in comparative analyses over the last decade. To address this issue, we propose a simple solution based on transforming the underlying variance-covariance matrix to adjust for model heterogeneity within PGLS. We suggest that heterogeneous rates of evolution might be particularly prevalent in large phylogenetic trees, while most current approaches assume a homogenous rate of evolution. Our analysis demonstrates that overlooking rate heterogeneity can result in inflated type I errors, thus misleading comparative analyses. We show that it is possible to correct for this bias even when the underlying model of evolution is not known a priori.

Deconstructing the relationships between phylogenetic diversity and ecology: a case study on ecosystem functioning.

Recent studies have supported a link between phylogenetic diversity and various ecological properties including ecosystem function. However, such studies typically assume that phylogenetic branches of equivalent length are more or less interchangeable. Here we suggest that there is a need to consider not only branch lengths but also their placement on the phylogeny. We demonstrate how two common indices of network centrality can be used to describe the evolutionary distinctiveness of network elements (nodes and branches) on a phylogeny. If phylogenetic diversity enhances ecosystem function via complementarity and the representation of functional diversity, we would predict a correlation between evolutionary distinctiveness of network elements and their contribution to ecosystem process. In contrast, if one or a few evolutionary innovations play key roles in ecosystem function, the relationship between evolutionary distinctiveness and functional contribution may be weak or absent. We illustrate how network elements associated with high functional contribution can be identified from regressions between phylogenetic diversity and productivity using a well-known empirical data set on plant productivity from the Cedar Creek Long-Term Ecological Research. We find no association between evolutionary distinctiveness and ecosystem functioning, but we are able to identify phylogenetic elements associated with species of known high functional contribution within the Fabaceae. Our perspective provides a useful guide in the search for ecological traits linking diversity and ecosystem function, and suggests a more nuanced consideration of phylogenetic diversity is required in the conservation and biodiversity-ecosystem-function literature.

Response to Strona & Fattorini: are generalist parasites being lost from their hosts?

We respond to criticism of our recent paper by examining assumptions about the structure of host-parasite networks, and discuss the implications of host extinction on our perception of parasite specificity.

Sickness behaviour associated with non-lethal infections in wild primates.

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

The path to host extinction can lead to loss of generalist parasites.

Host extinction can alter disease transmission dynamics, influence parasite extinction and ultimately change the nature of host-parasite systems. While theory predicts that single-host parasites are among the parasite species most susceptible to extinction following declines in their hosts, documented parasite extinctions are rare. Using a comparative approach, we investigate how the richness of single-host and multi-host parasites is influenced by extinction risk among ungulate and carnivore hosts. Host-parasite associations for free-living carnivores (order Carnivora) and terrestrial ungulates (orders Perissodactyla + Cetartiodactyla minus cetaceans) were merged with host trait data and IUCN Red List status to explore the distribution of single-host and multi-host parasites among threatened and non-threatened hosts. We find that threatened ungulates harbour a higher proportion of single-host parasites compared to non-threatened ungulates, which is explained by decreases in the richness of multi-host parasites. However, among carnivores threat status is not a significant predictor of the proportion of single-host parasites, or the richness of single-host or multi-host parasites. The loss of multi-host parasites from threatened ungulates may be explained by decreased cross-species contact as hosts decline and habitats become fragmented. Among carnivores, threat status may not be important in predicting patterns of parasite specificity because host decline results in equal losses of both single-host parasites and multi-host parasites through reduction in average population density and frequency of cross-species contact. Our results contrast with current models of parasite coextinction and highlight the need for updated theories that are applicable across host groups and account for both inter- and intraspecific contact.