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Biology subjects

Harrison, X. A.

Publications and source records attributed to Harrison, X. A..

10 recordsLinked to original sources

Examining interactions between the microbiome and viral infection across Drosophila species

Microbiomes can influence the outcomes of virus infection, while viral infections can disrupt microbiome composition. These reciprocal interactions may contribute to patterns of host susceptibility, but it remains unclear whether microbiome-virus interactions are consistent across host species, or whether host evolutionary relationships influence microbiome variation and its association with viral susceptibility. Here, we investigate interactions between bacterial microbiomes and Drosophila C virus (DCV) infection across 32 Drosophilidae host species, using experimental infections and 16S rRNA amplicon sequencing. Using phylogenetic mixed models, we tested for phylogenetic structure in microbiome diversity and composition, and whether specific bacterial taxa were associated with among-species variation in viral load. Drosophilidae microbiomes were consistently dominated by a small number of bacterial genera and showed limited phylogenetic structuring. DCV infection was associated with a small reduction in bacterial richness, but microbiome composition was only weakly affected by wounding or infection and largely dominated by within-species variation. However, specific taxa were associated with large differences in viral replication, including reduced DCV load in flies harbouring Streptococcus before infection or Bacillus during infection. These results suggest that, at least in the conditions used in this study, microbiome composition may not generate strong, generalisable host phylogenetic patterns in virus susceptibility.

evolutionary biology↗

Environment shapes the association between the skin microbiome and infection dynamics of the Dermocystid pathogen Amphibiothecum in Palmate newts (Lissotriton helveticus).

Infectious diseases are a leading cause of biodiversity declines, but the factors shaping the prevalence and intensity of wildlife disease outbreaks remain unresolved. Host-associated microbes are likely a key component of host resistance to infection, but a hosts ability to recruit such protective microbes may be restricted by the availability of microbes present in their immediate environment. Here we investigate the associations between the abiotic environment, skin microbiome, and infection with the Dermocystid pathogen Amphibiothecum meredithae in Palmate newts (Lissotriton helveticus) on the Isle of Rum, Scotland. We found more acidic ponds to be associated with higher skin microbiome diversity and lower pathogen prevalence. Predicted functional analysis of microbiota composition identified bacterially-mediated pathways linked to host immunity upregulated in skin microbiotas associated with more acidic ponds and lower infection prevalence. This study highlights the potential importance of the environment in modulating host- microbiome-pathogen relationships and patterns of infection in the wild.

ecology↗

Microbiome Dynamics During Translocation of the Critically-Endangered Frog Craugastor ranoides

O_LIAmphibian populations are declining and species going extinct due to habitat loss, climate change and emerging infectious disease, prompting the increasing use of translocations as a conservation tool. C_LIO_LISkin-associated microbial communities play a key role in amphibian health, particularly in protecting hosts from pathogenic infection. However, to date we know relatively little about the impact of translocation on the dynamics of skin-associated microbes, or the consequences of translocation-mediated disturbance of the microbiome for amphibian health. C_LIO_LIWe investigated the skin microbiome of the critically endangered frog Craugastor ranoides, now restricted to a fraction of its historical range in Costa Rica. We first conducted a multi-population survey to characterise among-population variation in skin bacterial communities. We then translocated individuals to a new site, using radio tracking to monitor them over time and assess individual-level changes in body mass, microbiome composition, and predicted microbial function. C_LIO_LIWe found limited among-population variation in skin microbiome composition across three different populations of C. ranoides. Response of the microbiome to translocation was highly individual-specific; some frogs demonstrated relatively stable community richness and composition, whilst others exhibited marked turnover in bacterial membership and predicted function. Body mass showed similar dynamics, but several of the recaptured frogs had gained mass after several days in the translocation site. C_LIO_LISynthesis and Applications: Our findings highlight the importance of considering microbiome dynamics in threatened species translocations to optimize individual health. This includes considering whether individuals should be prioritised for translocation based on their initial microbiome composition, and understanding how shifts in microbiome post-translocation may alter overall success of translocation efforts. These insights extend beyond amphibians, offering a broader framework for integrating long-term monitoring of host microbiomes and health into conservation efforts. C_LI

ecology↗

Lineage-specific trait variation generates widespread, contemporaneous coexistence and competitive exclusion dynamics in an invasive, multihost wildlife parasite

Invasive and highly virulent parasites are emerging worldwide, transported to new locations and into novel hosts by anthropogenic activities. Multiple introduction events lead to interactions amongst genetically dissimilar genotypes that can result in either competitive exclusion, coexistence, or cycling through a combination of the two. Here, we report how intra-lineage trait variation of the multihost amphibian parasite Batrachochytrium dendrobatidis drives contrasting outcomes of inter-lineage interactions on two continents, Europe and Africa. Through field surveys, competition experiments and mathematical modelling we show that interactions between the same two lineages in the two continents and in different hosts demonstrate both ends of the exclusion/coexistence continuum. Trait variation in one of the two predominating lineages, BdGPL, is responsible for these contrasting outcomes: In Europe, BdGPL is highly competitive and has constrained the distribution of the other, BdCAPE, to two locations. In Africa, BdGPL and BdCAPE can mutually invade host populations when the other lineage is already resident, potentially leading to coinfections and recombination. That these contrasting outcomes are prolonged and contemporaneous for the same two lineages shows that epidemiological models of invasive parasites need to account for trait variation both within and across lineages.

ecology↗

Spring temperature and land use change are associated with Rana temporaria reproductive success and phenology

Chemical pollution, land cover change, and climate change have all been established as important drivers of amphibian reproductive success and phenology. However, liQle is known about the relative impacts of these anthropogenic stressors, nor how they may interact to alter amphibian population dynamics. Addressing this gap in our knowledge is important, as it allows us to identify and prioritise the most needed conservation actions. Here, we use long-term datasets to investigate landscape-scale drivers of variation in the reproductive success and phenology of UK Common frog (Rana temporaria) populations. Consistent with predictions, we found that increasing mean temperatures resulted in clear advancements in amphibian breeding phenology: earlier congregation of breeding R. temporaria, earlier initialisation of spawning, and earlier hatching. Temperature and number of frost days also affected rates of spawn mortality. However, temperature increases were also strongly correlated with increases in urban area, arable area, and nitrate levels in the vicinity of spawning grounds. None of these variables could explain variation in the total surface area of spawn present at breeding sites. These findings support previous work linking warming temperatures to shiZ in amphibian breeding phenology, but also highlight the importance of assessing the effect of land use change and pollution on wild amphibian populations. These results have implications for our understanding of the response of wild amphibian populations to climate change, and the management of human-dominated landscapes for declining wildlife populations.

ecology↗

Older mothers produce offspring with longer telomeres: a longitudinal within-parent analysis

As telomere length often predicts survival and lifespan, there is considerable interest in understanding the origins of inter-individual variation in telomere length. Transgenerational effects of parental age on offspring telomere length are thought to be a key source of variation, but the rarity of longitudinal studies that examine the telomeres of successive offspring born throughout the lives of parents leaves such parental age effects poorly understood. Here, we exploit telomere length measures of successive offspring produced throughout the long breeding tenures of parents in wild white-browed sparrow-weaver (Plocepasser mahali) societies, to isolate the effects of within-parent changes in age on offspring telomere lengths. Our analyses reveal the first evidence to date of a positive within-parent effect of advancing age on offspring telomere length: as individual mothers age they produce offspring with longer telomeres. We consider the potential for pre- and post-natal mechanisms to explain our findings. As telomere erosion predicts offspring mortality in this species, this positive parental age effect could significantly impact parent and offspring fitness. Our findings support the view that transgenerational effects of parental age can be an appreciable source of inter-individual variation in telomere length.

evolutionary biology↗

Social environment drives sex and age-specific variation in Drosophila melanogaster microbiome composition and predicted function.

Social environments influence multiple traits of individuals including immunity, stress and ageing, often in sex-specific ways. The composition of the microbiome (the assemblage of symbiotic microorganisms within a host) is determined by environmental factors and the hosts immune, endocrine and neural systems. The social environment could alter host microbiomes extrinsically by affecting transmission between individuals, likely promoting homogeneity in the microbiome of social partners. Alternatively, intrinsic effects arising from interactions between the microbiome and host physiology (the microbiota-gut-brain axis) could translate social stress into dysbiotic microbiomes, with consequences for host health. We investigated how manipulating social environments during larval and adult life-stages altered the microbiome composition of Drosophila melanogaster fruit flies. We used social contexts that particularly alter the development and lifespan of males, predicting that any intrinsic social effects on the microbiome would therefore be sex-specific. The presence of adult males during the larval stage significantly altered the microbiome of pupae of both sexes. In adults, same-sex grouping increased bacterial diversity in both sexes. Importantly, the microbiome community structure of males was more sensitive to social contact at older ages, an effect partially mitigated by housing focal males with young rather than co-aged groups. Functional analyses suggest that these microbiome changes impact ageing and immune responses. This is consistent with the hypothesis that the substantial effects of the social environment on individual health are mediated through intrinsic effects on the microbiome, and provides a model for understanding the mechanistic basis of the microbiota-gut-brain axis. Significance statementThe social environment has pervasive, multifaceted effects on individual health and fitness. If a hosts microbiome is sensitive to the social environment then it could be an important mediator of social effects, as the reciprocal relationships between hosts and their microbiomes have substantial implications for host health. Using a Drosophila melanogaster fruit fly model we show that the fly microbiome is sensitive to the social environment in a sex, age and life-stage dependent manner. In particular, older adult male microbiome communities are altered by same-sex social contact, but this depends on the age of the social partners. These changes have functional effects on fly immunity and lifespan, evidence that indeed this is an influential mediator of social effects on health.

ecology↗

Captivity and exposure to the emerging fungal pathogen Batrachochytrium salamandrivorans are linked to perturbation and dysbiosis of the amphibian skin microbiome

O_LIThe emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal) is responsible for the catastrophic decline of European salamanders and poses a threat to amphibians globally.\nC_LIO_LIThe amphibian skin microbiome is strongly associated with disease outcome for several host-pathogen systems, yet its role in Bsal infection remains unresolved. In addition, many in-vivo Bsal studies to date have relied on specimens that have been kept in captivity for long periods without considering the influence of environment on the microbiome and how this may impact the host response to pathogen exposure.\nC_LIO_LIWe characterised the impact of captivity and exposure to Bsal on the skin bacterial and fungal communities of two co-occurring European newt species, the smooth newt (Lissotriton vulgaris) and the great-crested newt (Triturus cristatus).\nC_LIO_LIBsal infection and subsequent mortality in both newt species was associated with perturbation of the skin microbiome and possible dysbiosis. In addition, reduced microbial diversity and changes in microbiome structure accompanied the transition of newts from the wild to captivity, suggesting a possible decline in microbe-associated protection and increased risk of infection by opportunistic pathogens.\nC_LIO_LIOur findings advance current understanding of the role of host-associated microbiota in Bsal infection and highlight important considerations for ex-situ amphibian conservation programmes.\nC_LI

ecology↗

Disease mediated changes to life history and demography threaten the survival of European amphibian populations

Infectious diseases can influence the life history strategy of their hosts and such influences subsequently impact the demography of infected populations, reducing viability independently of increased mortality or morbidity. Amphibians are the most threatened group of vertebrates and emerging infectious diseases play a large role in their population declines. Viruses of genus Ranavirus are responsible for one of the deadliest of these diseases. To date no work has evaluated the impact of ranaviruses on host life-history post metamorphosis or population demographic structure at the individual level. In this study, we used skeletochronology and morphology to evaluate the impact of ranaviruses on the demography of populations of European common frog (Rana temporaria) in the United Kingdom. We compared ecologically similar populations that differed only in their historical presence or absence of ranaviral disease. Our results suggest that ranaviruses are associated with shifts in the age structure of infected populations, potentially caused by increased adult mortality and associated shifts in the life history of younger age classes. Population projection models indicate that such age truncation could heighten the vulnerability of frog populations to stochastic environmental challenges. Our individual level data provide further compelling evidence that the emergence of infectious diseases can alter host demography, subsequently increasing population vulnerability to additional stressors.

ecology↗

Host Microbiome Richness Predicts Resistance to Disturbance by Pathogenic Infection in a Vertebrate Host

Environmental heterogeneity is known to modulate the interactions between pathogens and hosts. However, the impact of environmental heterogeneity on the structure of host-associated microbial communities, and how these communities respond to pathogenic exposure remain poorly understood. Here we use an experimental framework to probe the links between environmental heterogeneity, skin microbiome structure and infection by the emerging pathogen Ranavirus in a vertebrate host, the European common frog (Rana temporaria). We provide evidence that environmental complexity directly influences the diversity and structure of the host skin microbiome, and that more diverse microbiomes are more resistant to perturbation associated with exposure to Ranavirus. Our data also indicate that host microbiome diversity covaries with survival following exposure to Ranavirus. Our study highlights the importance of extrinsic factors in driving host-pathogen dynamics in vertebrate hosts, and suggests that environment-mediated variation in the structure of the host microbiome may covary with observed differences in host susceptibility to disease in the wild.

ecology↗