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Explaining why some species are disproportionately impacted by the extinction crisis is of critical importance for conservation biology as a science and for proactively protecting species that are likely to become threatened in the future. Using the most current data on threat status, population trends, and threat types for 446 primate species, we advance previous research on the determinants of extinction risk by including a wider array of phenotypic traits as predictors, filling gaps in these trait data using multiple imputation, and investigating the mechanisms that connect organismal traits to extinction risk. Our Bayesian phylogenetically controlled analyses reveal that insular species exhibit higher threat status, while those that are more omnivorous and live in larger groups have lower threat status. The same traits are not linked to risk when repeating our analyses with older IUCN data, which may suggest that the traits influencing species risk are changing as anthropogenic effects continue to transform natural landscapes. We also show that non-insular, larger-bodied, and arboreal species are more susceptible to key threats responsible for primate population declines. Collectively, these results provide new insights to the determinants of primate extinction and identify the mechanisms (i.e. threats) that link traits to extinction risk.

Future biodiversity loss threatens the integrity of complex ecological associations, including among hosts and parasites. Almost half of primate species are threatened with extinction, and the loss of threatened hosts could negatively impact parasite associations and ecosystem functions. If endangered hosts are highly connected in host-parasite networks, then future host extinctions will also drive parasite extinctions, destabilizing ecological networks. If threatened hosts are not highly connected, however, then network structure should not be greatly affected by the loss of threatened hosts. Networks with high connectance, modularity, nestedness and robustness are more resilient to perturbations such as the loss of interactions than sparse, nonmodular and non-nested networks. We analysed the interaction network involving 213 primates and 763 parasites and removed threatened primates (114 species) to simulate the effects of extinction. Our analyses revealed that connections to 23% of primate parasites (176 species) may be lost if threatened primates go extinct. In addition, measures of network structure were affected, but in varying ways because threatened hosts have fewer parasite interactions than non-threatened hosts. These results reveal that host extinctions will perturb the host-parasite network and potentially lead to secondary extinctions of parasites. The ecological consequences of these extinctions remain unclear. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best-studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x̅ = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort-measured as the number of publications-had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism., (© 2019 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.)

Humans are thought to exhibit an unusual suite of life history traits relative to other primates, with a longer lifespan, later age at first reproduction, and shorter interbirth interval. These assumptions are key components of popular hypotheses about human life history evolution, but they have yet to be investigated phylogenetically. We applied two phylogenetic comparative methods to investigate whether these human life history traits differ from expectations based on other primates: one fits and selects between Brownian and Ornstein-Uhlenbeck models of trait evolution; the other tests for phylogenetic outliers by predicting phenotypic characteristics based on trait covariation and phylogeny for a species of interest. We found that humans have exceptionally short interbirth intervals, long lifespans, and high birth masses. We failed to find evidence that humans have a delayed age at first reproduction relative to body mass or other covariates. Overall, our results support several previous assertions about the uniqueness of human life history characteristics and the importance of cooperative breeding and socioecology in human life history evolution. However, we suggest that several hypotheses about human life history need to be revised in light of our finding that humans do not have a delayed age at first reproduction., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

Objectives: Primates vary in their sleep durations and, remarkably, humans sleep the least per 24-hr period of the 30 primates that have been studied. Using phylogenetic methods that quantitatively situate human phenotypes within a broader primate comparative context, we investigated the evolution of human sleep architecture, focusing on: total sleep duration, rapid eye movement (REM) sleep duration, non-rapid eye movement (NREM) sleep duration, and proportion of sleep in REM., Materials and Methods: We used two different Bayesian methods: phylogenetic prediction based on phylogenetic generalized least squares and a multistate Onrstein-Uhlenbeck (OU) evolutionary model of random drift and stabilizing selection., Results: Phylogenetic prediction confirmed that humans sleep less than predicted for a primate of our body mass, predation risk, brain size, foraging needs, sexual selection, and diet. These analyses further revealed that humans pack an unexpectedly higher proportion of REM sleep within a shorter overall sleep duration, and do so by reducing NREM sleep (rather than increasing REM). The OU model generally confirmed these findings, with shifts along the human lineage inferred for TST, NREM, and proportion of REM, but not for REM., Discussion: We propose that the risks and opportunity costs of sleep are responsible for shorter sleep durations in humans, with risks arising from terrestrial sleep involving threats from predators and conspecifics, and opportunity costs because time spent sleeping could be used for learning, creating material objects, and socializing., (© 2018 Wiley Periodicals, Inc.)

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Objectives: The ongoing risk of emerging infectious disease has renewed calls for understanding the origins of zoonoses and identifying future zoonotic disease threats. Given their close phylogenetic relatedness and geographic overlap with humans, non‐human primates (NHPs) have been the source of many infectious diseases throughout human evolution. NHPs harbor diverse parasites, with some infecting only a single host species while others infect species from multiple families. Materials and Methods: We applied a novel link‐prediction method to predict undocumented instances of parasite sharing between humans and NHPs. Our model makes predictions based on phylogenetic distances and geographic overlap among NHPs and humans in six countries with high NHP diversity: Columbia, Brazil, Democratic Republic of Congo, Madagascar, China, and Indonesia. Results: Of the 899 human parasites documented in the Global Infectious Diseases and Epidemiology Network (GIDEON) database for these countries, 12% were shared with at least one other NHP species. The link prediction model identified an additional 54 parasites that are likely to infect humans but were not reported in GIDEON. These parasites were mostly host generalists, yet their phylogenetic host breadth varied substantially. Discussion: As human activities and populations encroach on NHP habitats, opportunities for parasite sharing between human and NHPs will continue to increase. Our study identifies specific infectious organisms to monitor in countries with high NHP diversity, while the comparative analysis of host generalism, parasite taxonomy, and transmission mode provides insights to types of parasites that represent high zoonotic risk. [ABSTRACT FROM AUTHOR]

Explaining why some species are disproportionately impacted by the extinction crisis is of critical importance for conservation biology as a science and for proactively protecting species that are likely to become threatened in the future. Using the most current data on threat status, population trends, and threat types for 446 primate species, we advance previous research on the determinants of extinction risk by including a wider array of phenotypic traits as predictors, filling gaps in these trait data using multiple imputation, and investigating the mechanisms that connect organismal traits to extinction risk. Our Bayesian phylogenetically controlled analyses reveal that insular species exhibit higher threat status, while those that are more omnivorous and live in larger groups have lower threat status. The same traits are not linked to risk when repeating our analyses with older IUCN data, which may suggest that the traits influencing species risk are changing as anthropogenic effects continue to transform natural landscapes. We also show that non-insular, larger-bodied, and arboreal species are more susceptible to key threats responsible for primate population declines. Collectively, these results provide new insights to the determinants of primate extinction and identify the mechanisms (i.e. threats) that link traits to extinction risk. [ABSTRACT FROM AUTHOR]

Parasites regularly switch into new host species, representing a disease burden and conservation risk to the hosts. The distribution of these parasites also gives insight into characteristics of ecological networks and genetic mechanisms of host-parasite interactions. Some parasites are shared across many species, whereas others tend to be restricted to hosts from a single species. Understanding the mechanisms producing this distribution of host specificity can enable more effective interventions and potentially identify genetic targets for vaccines or therapies. As ecological connections between human and local animal populations increase, the risk to human and wildlife health from novel parasites also increases. Which of these parasites will fizzle out and which have the potential to become widespread in humans? We consider the case of primate malarias, caused by Plasmodium parasites, to investigate the interacting ecological and evolutionary mechanisms that put human and nonhuman primates at risk for infection. Plasmodium host switching from nonhuman primates to humans led to ancient introductions of the most common malaria-causing agents in humans today, and new parasite switching is a growing threat, especially in Asia and South America. Based on a wild host-Plasmodium occurrence database, we highlight geographic areas of concern and potential areas to target further sampling. We also discuss methodological developments that will facilitate clinical and field-based interventions to improve human and wildlife health based on this eco-evolutionary perspective. [ABSTRACT FROM AUTHOR]

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations. [ABSTRACT FROM AUTHOR]

Cathemerality, or activity throughout the 24-hr cycle, is rare in primates yet relatively common among lemurs. However, the diverse ecological conditions under which cathemerality is expressed complicates attempts to identify species-typical behavior. For example, Lemur catta and Varecia have historically been described as diurnal, yet recent studies suggest that they might exhibit cathemeral behavior under some conditions. To investigate this variation, we monitored activity patterns among lemurs that are exposed to similar captive environments. Using MotionWatch 8 ® actigraphy data loggers, we studied 88 lemurs across seven species at the Duke Lemur Center (DLC). Six species were members of the family Lemuridae ( Eulemur coronatus, E. flavifrons, E. mongoz, L. catta, V. rubra, V. variegata), while a seventh was strictly diurnal and included as an out-group ( Propithecus coquereli). For each 24-hr cycle ( N = 503), we generated two estimates of cathemerality: mean night (MN) activity and day/night (DN) activity ratio (day and night cutoffs were based on astronomical twilights). As expected, P. coquereli engaged in the least amount of nocturnal activity according to both measures; their activity was also outside the 95% confidence intervals of all three cathemeral Eulemur species, which exhibited the greatest evidence of cathemerality. By these estimates, Varecia activity was most similar to Eulemur and exhibited substantial deviations from P. coquereli (β (MN) = 0.22 ± SE 0.12; β (DN) = −0.21 ± SE 0.12). L. catta activity patterns also deviated from P. coquereli (β (MN) = 0.12 ± SE 0.11; β (DN) = −0.15 ± SE 0.12) but to a lesser degree than either Varecia or Eulemur. Overall, L. catta displayed an intermediate activity pattern between Eulemur and P. coquereli, which is somewhat consistent with wild studies. Regarding Varecia, although additional observations in more diverse wild habitats are needed, our findings support the existence of cathemeral behavior in this genus. [ABSTRACT FROM AUTHOR]

Illuminating the ecological and evolutionary dynamics of parasites is one of the most pressing issues facing modern science, and is critical for basic science, the global economy, and human health. Extremely important to this effort are data on the disease-causing organisms of wild animal hosts (including viruses, bacteria, protozoa, helminths, arthropods, and fungi). Here we present an updated version of the Global Mammal Parasite Database, a database of the parasites of wild ungulates (artiodactyls and perissodactyls), carnivores, and primates, and make it available for download as complete flat files. The updated database has more than 24,000 entries in the main data file alone, representing data from over 2700 literature sources. We include data on sampling method and sample sizes when reported, as well as both 'reported' and 'corrected' (i.e., standardized) binomials for each host and parasite species. Also included are current higher taxonomies and data on transmission modes used by the majority of species of parasites in the database. In the associated metadata we describe the methods used to identify sources and extract data from the primary literature, how entries were checked for errors, methods used to georeference entries, and how host and parasite taxonomies were standardized across the database. We also provide definitions of the data fields in each of the four files that users can download. [ABSTRACT FROM AUTHOR]

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans. [ABSTRACT FROM AUTHOR]