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Biology subjects

Albery, G. F.

Publications and source records attributed to Albery, G. F..

At least 19 recordsLinked to original sources

Local density shapes complete brood failure across species boundaries in two sympatric songbirds

Reproduction in species with parental care involves sustaining a brood of offspring through an energetically demanding period, when shifts in resource availability, weather, predation risk, and parental condition can strongly alter offspring survival. The most extreme outcome is complete brood failure (death of all offspring), which is relatively frequent in many bird species and may occur when conditions cross a viability threshold. Although complete brood failure is important for shaping fitness variation and population dynamics, we have limited understanding of how intra- and interspecific density dependence governs these events, or of how factors such as habitat quality and disease burden contribute to them, because deriving this requires fine-scale, individual-level data collected across generations for multiple overlapping species. Using a dataset totalling 38,509 nesting attempts from great tits (Parus major) and blue tits (Cyanistes caeruleus) in Wytham Woods, Oxford, UK, we examined how brood failure is shaped by local conspecific and heterospecific density, habitat structure, and avian malaria infection for a subset. Complete brood failure was frequent (14.75%), mostly involving chick mortality in the nest consistent with starvation, rather than brood removal by predators. Relationships between density and brood failure were strong but species-specific. Specifically, great tit failure risk was higher in neighbourhoods that remained densely populated across years, whereas blue tit failure risk was lower where annual great tit or combined density was high, but not where annual blue tit density itself was high. This suggests that local overall density reflects continuing constraint for great tits, while local annual density may partly track favourable within-year conditions and settlement patterns for blue tits. In great tits, failure was also more common where oak density was low and farther from the closest river (Thames), while habitat associations were weak in blue tits. Malaria infection was spatially heterogeneous and covaried with density and habitat, but infection status did not significantly explain complete brood failure. Together, these results show that complete brood failure is shaped by spatially structured local ecological context, and how density dependence in these events can differ in direction and timescale between sympatric species.

ecology↗

Fitness costs of parasitism depend on fine-scale density and resource availability in a wild ungulate

Resource competition and parasite exposure both present common density-dependent fitness costs for wild animals. Because launching effective immune responses is costly in terms of resources, parasites fitness costs should be further exacerbated in high-density, resource-depleted areas. To disentangle these relationships, we related density, parasitism, and resource availability to survival and fecundity across lifespan in a long-term study of wild red deer. All fitness measures declined with a combination of parasite count, greater density, and reduced resource availability. Beyond these relationships, as expected, local density and resource scarcity exacerbated survival costs of parasitism in calves, effectively undermining tolerance of infection. However, these synergistic relationships faded in yearlings and then reversed in adults, likely through age-structured selection biases. These findings emphasize that the costs of parasites and resource scarcity can be synergistic and intertwined with density in wild populations, accentuating the value of incorporating resource competition when examining parasite-dependent population regulation.

ecology↗

Resource supplementation alters host exposure, susceptibility, and infection dynamics across a diverse parasite community

Resource availability is crucial in shaping exposure and resistance to parasites. Although effects are expected to vary across parasite species, most of our knowledge comes from single-host, single-parasite studies. In a wild wood mouse population (Apodemus sylvaticus), we supplemented dietary resources over 3 years and quantified effects on a diverse parasite community alongside host behaviour and physiology. Resource supplementation had diverse impacts on 12 parasite taxa including positive (3/12), negative (6/12), and null (3/12) results. Supplementation also influenced host biology, with supplemented mice moving less, experiencing higher conspecific densities, improved conditions, and increased reproduction. These findings experimentally demonstrate that resource availability can multifacetedly affect disease dynamics. The complexity likely arises due to combined effects on exposure and susceptibility processes. Our study advances understanding of disease drivers at the human-wild interface and underscores the importance of assessing whole parasite communities to predict responses to changing resource landscapes in the wild.

ecology↗

Museum collections and machine learning guide discovery of novel coronaviruses and paramyxoviruses

Natural history museum collections are valuable but underutilized resources for viral discovery, offering opportunities to test hypotheses about viral occurrence across space, time, and taxonomic groups. We developed machine learning models of bat host suitability to guide coronavirus and paramyxovirus screening of 1330 and 491 tissues, respectively, in a museum collection. For the first time, we recovered coronavirus (n = 16) and paramyxovirus (n = 3) sequences from archived museum tissues, confirming three novel coronavirus host species and three novel paramyxovirus host species (3% and 33% prediction success rate, respectively). These sequences included a SARS-like coronavirus and an orthoparamyxovirus from Angolan Rhinolophus fumigatus specimens collected in June 2019, suggesting that viruses with epidemic potential may be more widespread in sub-Saharan Africa than previously believed. Our study demonstrates the value of combining predictive modeling and collections-based viral discovery, particularly for filling outstanding sampling gaps and investigating changes in host-virus associations over time.

ecology↗

Environment dependent benefits of sociality in Soay sheep

An individuals social connections have strong effects on fitness. Despite this, there is pronounced among-individual variation in social behaviour. This variation may be maintained if different types of social connections have environment-dependent fitness benefits, but this has rarely been tested. We applied network analysis to 37 years of social association data in Soay sheep to test this hypothesis. Our results show that both relationship quantity (having many association partners) and relationship quality (having strong associations) are linked with survival. Crucially, the relative importance of relationship quantity and quality depends on overwinter weather, with harsh conditions favouring quantity over quality, likely due to thermoregulatory benefits. Relationship quality, meanwhile, was most beneficial under benign weather conditions, possibly due to enhanced familiarity with conspecifics. These findings advance our understanding of social benefits in fission-fusion societies and show that changing environmental conditions may be an important mechanism maintaining variation in social behaviour in natural populations.

animal behavior and cognition↗

Parasite-mediated inbreeding depression in wild red deer

Inbreeding depression is the reduction in fitness of inbred individuals relative to their more outbred counterparts. Parasitism also reduces fitness and is a route by which inbreeding depression may operate, yet the complete pathway from inbreeding to parasitism to fitness has almost never been documented in the wild. Using high-quality, individual-level data on fitness in juveniles and adult females, longitudinal infection data for three gastrointestinal helminth parasites, and genomic inbreeding coefficients we test for parasite-mediated inbreeding depression in a wild ungulate population (red deer, Cervus elaphus). We found evidence for parasite-mediated inbreeding depression via strongyle nematodes in juvenile survival, independent of direct adverse effects of inbreeding on survival and indirect effects of inbreeding on survival via birth weight. Inbreeding also reduced fitness in reproductive adults by reducing overwinter survival. Our study reveals three independent pathways by which inbreeding depresses fitness and highlights the rarely-studied route of parasitism.

ecology↗

Population density drives increased parasitism via greater exposure and reduced resource availability in wild hosts

Exposure to environmental parasites should increase with host population density due to the accumulation of infective parasites in space. However, competition for resources also increases with density, lowering condition and increasing susceptibility, which offers an alternative pathway for density-dependent infection to act. To test how these two processes act independently or together to drive greater parasite counts, we used a long-term study of red deer to examine associations between host density, resource availability, and counts of three common helminth parasites. We found that greater density correlated with reduced resource availability, and while density was positively associated with both strongyle and tissue worm burdens, resource availability was independently and negatively associated with the same burdens, supporting separate roles of density-dependent exposure and susceptibility in driving infection. This study provides evidence that competition for resources is an important driver of infection in higher-density areas, exacerbating the effects of density-dependent increases in exposure.

ecology↗

Density-dependent network structuring within and across wild animal systems

High population density should drive individuals to more frequently share space and interact, producing better-connected spatial and social networks [1-4]. Although this theory is fundamental to our understanding of disease dynamics [2,5-8], it remains unconfirmed how local density generally drives individuals positions within their networks, which reduces our ability to understand and predict density-dependent processes [4,9,10]. Here we provide the first general evidence that density drives greater network connectedness at fine spatiotemporal scales, at the scale of individuals within wild animal populations. We analysed 36 datasets of simultaneous spatial and social behaviour in >58,000 individual animals, spanning 30 species of fish, reptiles, birds, mammals, and insects. 80% of systems exhibited strong positive relationships between local density and network centrality. However, >80% of relationships were nonlinear and 75% became shallower at higher values, signifying that demographic and behavioural processes counteract densitys effects, thereby producing saturating trends [11-15]. Densitys effect was much stronger and less saturating for spatial than social networks, such that individuals become disproportionately spatially connected rather than socially at higher densities. Consequently, ecological processes that depend on spatial connections (e.g. indirect pathogen transmission, resource competition, and territory formation) are likely more density-dependent than those involving social interactions (e.g. direct pathogen transmission, aggression, and social learning). These findings reveal fundamental ecological rules governing societal structuring, with widespread implications. Identifying scaling rules based on processes that generalise across systems, such as these patterns of density dependence, might provide the ability to predict network structures in novel systems.

ecology↗

Local and global density have distinct and parasite-dependent effects on infection in wild sheep

High density should drive greater parasite exposure. However, evidence linking density with infection generally uses density proxies, rather than of individuals per space within a continuous population. We used a long-term study of wild sheep to link within-population spatiotemporal variation in host density with individual parasite counts. Although four parasites exhibited strong positive relationships with local density, these relationships were mostly restricted to juveniles and faded in adults. Further, one ectoparasite showed strong negative relationships across all age classes. In contrast, population size - a measure of global density - had limited explanatory power, and its effects did not remove those of spatial density, but were complementary. These results indicate that local and global density can exhibit diverse and contrasting effects on infection within populations. Spatial measures of within-population local density may provide substantial additional insight to temporal metrics based on population size, and investigating them more widely could be highly revealing.

ecology↗

Different types of social links contrastingly shape reproductive wellbeing in a multi-level society of wild songbirds

The social environment has diverse consequences for individuals welfare, health, reproductive success, and survival. This environment consists of different kinds of dyadic bonds that exist at different levels; in many social species, smaller social units come together in larger groups, creating multilevel societies. In great tits (Parus major), individuals have four major types of dyadic bonds: pair mates, breeding neighbours, flockmates, and spatial associates, all of which have been previously linked to fitness outcomes. Here, we show that these different types of dyadic bonds are differentially linked with subsequent reproductive success metrics in this wild population and that considering spatial effects provides further insights into these relationships. We provide evidence that more social individuals had a higher number of fledglings, and individuals with more spatial associates had smaller clutch sizes. We also show individuals with stronger bonds with their pair mate had earlier lay dates. Our study highlights the importance of considering different types of dyadic relationships when investigating the relationship between wellbeing and sociality, and the need for future work aimed at experimentally testing these relationships, particularly in spatially structured populations.

ecology↗

Social responses to a hurricane drive greater epidemic risk

Climate change is intensifying extreme weather events, with severe implications for ecosystem dynamics. A key behavioural mechanism whereby animals may cope with such events is by increasing social cohesion to improve access to scarce resources like refuges, which in turn could exacerbate epidemic risk due to increased close contact. However, how and to what extent natural disasters affect disease risk via changes in sociality remains unexplored in animal populations. By modelling disease spread in free-living rhesus macaque groups (Macaca mulatta) before and after a hurricane, we demonstrate doubled pathogen transmission rates up to five years following the disaster, equivalent to an increase in pathogen infectivity from 10% to 20%. Moreover, the hurricane redistributed the risk of infection across the population, decreasing status-related differences found in pre-hurricane years. These findings demonstrate that natural disasters can exacerbate and homogenise epidemic risk in an animal population via changes in sociality. These observations provide unexpected further mechanisms by which extreme weather events can threaten wildlife health, population viability, and spillover to humans.

ecology↗

Different helminth parasites show contrasting relationships with age in a wild ungulate

As animals age they often exhibit substantial physiological and behavioural changes that can drive changes in infection status over the lifespan. Generally, immunosenescence is expected to lead to greater infection in older individuals, but this process could be confounded or counteracted by changes in behaviour, selective disappearance of certain individuals, or a range of immune processes. Here, we uncover contrasting age-related patterns of infection across three different helminth parasites in wild adult red deer (Cervus elaphus). Counts of strongyle nematodes (order: Strongylida) increased with age, while counts of liver fluke (Fasciola hepatica) and tissue worm (Elaphostrongylus cervi) decreased. These relationships could not be explained by selective disappearance of certain individuals or changes in behaviour, suggesting that immune changes could be responsible. Additionally, we found a positive relationship between social connectedness and strongyle infection, implying that previously documented age-related decreases in social behaviour may minimise exposure, reducing the negative effects of immunosenescence. These findings demonstrate that burdens of different parasites can show contrasting changes over an individuals lifespan depending on a complex suite of intrinsic and extrinsic factors.

ecology↗

Ecological drivers of sustained enzootic yellow fever virus transmission in Brazil, 2017-2021

Beginning December 2016, sylvatic yellow fever (YF) outbreaks spread into southeastern Brazil, and Minas Gerais state experienced two sylvatic YF waves (2017 and 2018). Following these massive YF waves, we screened 187 free-living non-human primate (NHPs) carcasses collected throughout the state between January 2019 and June 2021 for YF virus (YFV) using qPCR. One sample belonging to a Callithrix, collected in June 2020, was positive for YFV. The viral strain belonged to the same lineage associated with 2017-2018 outbreaks, showing the continued enzootic circulation of YFV in the state. Next, using data from 781 NHPs carcasses collected in 2017-18, we used generalized additive mixed models (GAMMs) to identify the spatiotemporal and host-level drivers of YFV infection and intensity (an estimation of genomic viral load in the liver of infected NHP). Our GAMMs explained 65% and 68% of variation in virus infection and intensity, respectively, and uncovered strong temporal and spatial patterns for YFV infection and intensity. NHP infection was higher in the eastern part of Minas Gerais state, where 2017-2018 outbreaks affecting humans and NHPs were concentrated. The odds of YFV infection were significantly lower in NHPs from urban areas than from urban-rural or rural areas, while infection intensity was significantly lower in NHPs from urban areas or the urban-rural interface relative to rural areas. Both YFV infection and intensity were higher during the warm/rainy season compared to the cold/dry season. The higher YFV intensity in NHPs in warm/rainy periods could be a result of higher exposure to vectors and/or higher virus titers in vectors during this time resulting in the delivery of a higher virus dose and higher viral replication levels within NHPs. Further studies are needed to better test this hypothesis and further compare the dynamics of YFV enzootic cycles between different seasons. Author SummaryIn 2017 and 2018 massive sylvatic yellow fever (YF) outbreaks took place in Minas Gerais Brazil. To investigate yellow fever virus (YFV) circulation following these massive outbreaks, we investigated samples from 187 free-living non-human primate (NHPs) collected between January 2019 and June 2021. One sample belonging to a Callithrix, collected in June 2020 was positive for YFV. This virus was closely related to YFV from previous outbreaks (2017-2018) showing the continued enzootic circulation of YFV in the state. Next, we investigated the drivers of YFV infection and intensity (an estimation of viral load in each infected NHP) during the 2017-18 outbreaks. The odds of YFV infection in NHPs were lower in urban areas compared to rural ones as expected in sylvatic cycles. There were strong temporal and spatial patterns were observed for YFV infection and intensity, especially in the eastern part of Minas Gerais state. The higher YFV infection and intensity observed during the warm/rainy season (as opposed to the cold/dry one) could be related to higher exposure to vectors and/or higher virus titers in vectors during this time. The possible delivery of a higher virus dose in NHPs could lead to higher viral replication levels within NHPs explaining the higher intensity of infection during warm/rainy season. Further studies are needed to better test this hypothesis and further compare the dynamics of YFV enzootic cycles between different seasons.

microbiology↗

Pathogen transmission modes determine contact network structure, altering other pathogen characteristics

Pathogen traits can vary greatly and impact the ability of a pathogen to persist in a population. Although this variation is fundamental to disease ecology, little is known about the evolutionary pressures that drive these differences, particularly where they interact with host behavior. We hypothesized that host behaviors relevant to different transmission routes give rise to differences in contact network structure, constraining the space over which pathogen traits can evolve to maximize fitness. Our analysis of 232 contact networks across mammals, birds, reptiles, amphibians, arthropods, fish, and mollusks found that contact network topology varies by contact events, most notably in networks that are representative of fluid-exchange transmission. Using infectious disease model simulations, we showed that these differences in network structure suggest pathogens transmitted through fluid-exchange contact events will need traits associated with high transmissibility to successfully proliferate, compared to pathogens that transmit through other types of contact. These findings were supported through a review of known traits of pathogens that transmit in humans. Our work demonstrates that contact network structure may drive the evolution of compensatory pathogen traits according to transmission strategy, providing essential context for understanding pathogen evolution and ecology.

evolutionary biology↗

Viral diversity and zoonotic risk in endangered species

A growing body of evidence links zoonotic disease risk, including pandemic threats, to biodiversity loss and other upstream anthropogenic impacts on ecosystem health. However, there is little current research assessing viral diversity in endangered species. Here, combining IUCN Red List data on 5,876 mammal species with data on host-virus associations for a subset of 1,273 extant species, we examine the relationship between endangered species status and viral diversity, including the subset of viruses that can infect humans (zoonotic viruses). We show that fewer total viruses and fewer zoonotic viruses are known to infect more threatened species. After correcting for sampling effort, zoonotic virus diversity is mostly independent of threat status, but endangered species--despite a higher apparent research effort--have a significantly lower diversity of viruses, a property that is not explained by collinearity with host phylogeography or life history variation. Although this pattern could be generated by real biological processes, we suspect instead that endangered species may be subject to additional sampling biases not captured by the total volume of scientific literature (e.g., lower rates of invasive sampling may decrease viral discovery). Overall, our findings suggest that endangered species are no more or less likely to host viruses that pose a threat to humans, but future zoonotic threats might remain undiscovered in these species. This may be concerning, given that drivers of endangered species vulnerability such as habitat disturbance, wildlife trade, or climate vulnerability may increase virus prevalence in reservoirs and risk of spillover into humans.

ecology↗

Understanding spatiotemporal effects of food supplementation on host-parasite interactions using community-based science

O_LISupplemental feeding can increase the overall health of animals but also can have variable effects on how animals defend themselves against parasites. However, the spatiotemporal effects of food supplementation on host-parasite interactions remain poorly understood, likely because large-scale, coordinated efforts are difficult. C_LIO_LIHere, we introduce the Nest Parasite Community Science Project, which is a community-based science project that coordinates studies with bird nest box "stewards" from the public and scientific community. This project was established to understand broad ecological patterns between hosts and their parasites. C_LIO_LIThe goal of this study was to determine the effect of food supplementation on eastern bluebirds (Sialia sialis) and their nest parasite community across the geographic range of the bluebirds from 2018-2021. We received 646 nests from 68 stewards in 26 states in the eastern United States. Nest box stewards reported whether or not they fed their bluebirds mealworms or suet, then followed the nesting success of the birds (number of eggs laid and hatched, percent hatched, number and percent fledged). We then identified and quantified parasites in the nests. C_LIO_LIWe found that food supplementation increased fledgling numbers and proportional fledging success. The main nest parasite taxa were parasitic blow flies (Protocalliphora sialia), but a few nests contained fleas (Ceratophyllus idius, C. gallinae, Orchopeas leucopus) and mites (Dermanyssus spp. and Ornithonyssus spp.). Blow flies were primarily found at northern latitudes, where food supplementation affected blow fly abundance. However, the direction of this effect varied substantially in direction and magnitude across years. More stewards fed bluebirds at southern latitudes than at northern latitudes, which contradicted the findings of other community-based science projects. C_LIO_LIOverall, food supplementation of birds was associated with increased host fitness but did not appear to play a consistent role in defense against these parasites across all years. Our study demonstrates the importance of coordinated studies across years and locations to understand the effects of environmental heterogeneity, including human-based food supplementation, on host-parasite dynamics. Studies during a single year or considering only a single population might not provide the necessary data to develop management strategies for species. C_LI

ecology↗

Novel pathogen introduction rapidly alters evolved movement strategies, restructuring animal societies

Animal sociality emerges from individual decisions on how to balance the costs and benefits of being sociable. Movement strategies incorporating social information -- the presence and status of neighbours -- can modulate spatial associations, helping animals avoid infection while benefiting from indirect information about their environment. When a novel pathogen is introduced into a population, it should increase the costs of sociality, selecting against gregariousness. Yet current thinking about novel pathogen introductions into wildlife neglects hosts potential evolutionary responses. We built an individual-based model that captures essential features of the repeated introduction, and subsequent transmission of an infectious pathogen among social hosts. Examining movements in a foraging context, widely shared by many species, we show how introducing a novel pathogen to a population provokes a rapid evolutionary transition to a dynamic social distancing movement strategy. This evolutionary shift triggers a disease-dominated ecological cascade of increased individual movement, decreased resource harvesting, and fewer social encounters. Pathogen-risk adapted individuals form less clustered social networks than their pathogen-risk naive ancestors, which reduces the spread of disease. The mix of post-introduction social movement strategies is influenced by the usefulness of social information and disease cost. Our work demonstrates that evolutionary adaptation to pathogen introductions and re-introductions can be very rapid, comparable to ecological timescales. Our general modelling framework shows why evolutionary dynamics should be considered in movement-disease models, and offers initial predictions for the eco-evolutionary consequences of wildlife pathogen spillover scenarios.

ecology↗

The epidemiology and genomics of a virulent emerging fungal pathogen in an Australian reptile

Emerging infectious fungal diseases (EIFDs) represent a major conservation concern worldwide. Here, we provide early insights into the potential threat that Nannizziopsis barbatae (Nb), a novel EIFD, poses to Australian herpetological biodiversity. First known to the reptile pet trade as a primary pathogen causing untreatable severe dermatomycosis, since 2013, Nb has emerged in a growing number of phylogenetically and ecologically distant free-living reptiles across Australia. Observing its emergence in a long-term study population of wild eastern water dragons (Intellagama lesueurii), we demonstrate the pathogens virulence-related genomic features, within-population spatiotemporal spread, and survival costs, all of which imply that Nb could pose a threat to Australian reptiles in the future. Our findings highlight the need to closely monitor this pathogen in Australian ecosystems.

ecology↗