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McCallum, H.

Publications and source records attributed to McCallum, H..

9 recordsLinked to original sources

Response to "No evidence that transmissible cancer has shifted from emergence to endemism in Tasmanian devils"

Herein, we rebut the critique of Patton et al. (2020), entitled, "No evidence that a transmissible cancer has shifted from emergence to endemism", by Stammnitz et al. (2024). First and foremost, the authors do not conduct any phylogenetic or epidemiological analyses to rebut the inferences from the main results of the Patton et al. (2020) article, rendering the title of their rebuttal without evidence or merit. Additionally, Stammnitz et al. (2024) present a phylogenetic tree based on only 32 copy number variants (not typically used in phylogenetic analyses and evolve in a completely different way than DNA sequences) to "rebut" our tree that was inferred from 436.1 kb of sequence data and nearly two orders of magnitude more parsimony-informative sites (2520 SNPs). As such it is not surprising that their phylogeny did not have a similar branching pattern to ours, given that support for each branch of their tree was weak and the essentially formed a polytomy. That is, one could rotate their resulting tree in any direction and by nature, it would not match ours. While the authors are correct that we used suboptimal filtering of our raw whole genome sequencing data, re-analyses of the data with 30X coverage, as suggested, resulted in a mutation rate similar to that reported in Stammnitz et al. (2024). Most importantly, when we re-analyzed our data, as well as Stammnitz et al.s own data, the results of the Patton et al. (2020) article are supported with both datasets. That is, the effective transmission rate of DFTD has transitioned over time to approach one, suggesting endemism; and, the spread of DFTD is rapid and omnidirectional despite the observed east-to-west wave of spread. Overall, Stammnitz et al. (2024) not only fail to provide evidence to contradict the findings of Patton et al. (2020), but rather help support the results with their own data.

evolutionary biology↗

Effects of a transmissible cancer on life-history traits in Tasmanian devils

Shifts in life history traits, such as timing of reproduction, can help mediate population declines following perturbations, and early reproduction should be favoured when adult survival is impacted more than juvenile survival. In Tasmanian devils, following the emergence of a fatal transmissible cancer, females started to breed precocially (i.e., at age one instead of typically age two) and the same time as populations started to decline following disease emergence. Here, we focus on a diseased site (Freycinet Peninsula, Tasmania, Australia) with 18 years of continuous mark-recapture data to test: (1) whether rates of precocial breeding in females continued to increase after the initial rise after the emergence of the disease, (2) whether there was a relationship between body size and breeding success for either one-year-olds or adult females (i.e., at least two-years-old), and (3) whether there was inbreeding depression in breeding success for either age category. We show that rates of precocial breeding did not continue to rise, and that the proportion of precocially breeding females has plateaued at around 50%. We also show that there was no effect of body size on the probability of breeding for either one-year-old or for adult females. Finally, we show that there was no evidence for inbreeding depression in breeding success for either age class. We discuss possible constraints that may have inhibited further rise in rates of precocial breeding in the context of limitations to growth in the offspring of precocially breeding (and therefore smaller) females.

evolutionary biology↗

Periodic shifts in viral load increase risk of spillover from bats

Prediction and management of zoonotic pathogen spillover requires an understanding of infection dynamics within reservoir host populations. Transmission risk is often assessed using prevalence of infected hosts, with infection status based on the presence of genomic material. However, detection of viral genomic material alone does not necessarily indicate the presence of infectious virus, which could decouple prevalence from transmission risk. We undertook a multi-faceted investigation of Hendra virus shedding in Pteropus bats, combining insights from virus isolation, viral load proxies, viral prevalence, and longitudinal patterns of shedding, from 6,151 samples. In addition to seasonal and interannual fluctuation in prevalence, we found evidence for periodic shifts in the distribution of viral loads. The proportion of bats shedding high viral loads was higher during peak prevalence periods during which spillover events were observed, and lower during non-peak periods when there were no spillovers. We suggest that prolonged periods of low viral load and low prevalence reflect prolonged shedding of non-infectious RNA, or viral loads that are insufficient or unlikely to overcome dose barriers to spillover infection. These findings show that incorporating viral load (or proxies of viral load) into longitudinal studies of virus excretion will better inform predictions of spillover risk than prevalence alone. Significance statementWe present a comprehensive analysis of a high-profile bat-virus system (Hendra virus in Australian flying-foxes) to demonstrate that both prevalence and viral loads can shift systematically over time, resulting in concentrated periods of increased spillover risk when prevalence and viral loads are high. We further suggest that prolonged periods of low-prevalence, low-load shedding may not reflect excretion of infectious virus, resolving the outstanding puzzle of why spillovers have not been observed during periods of low off-season prevalence in subtropical Australia, or more frequently in tropical Australia despite consistent low-prevalence shedding. The consideration of viral loads (or proxies of viral load) along with prevalence may improve risk inference from longitudinal surveys of zoonotic viruses across wildlife reservoir hosts.

ecology↗

Physiology and ecology combine to determine host and vector importance for Ross River virus and other vector-borne diseases

Identifying the key vector and host species driving transmission is notoriously difficult for vector-borne zoonoses, but critical for disease control. Here, we present a general approach for quantifying the role hosts and vectors play in transmission that integrates species physiological competence with their ecological traits. We apply this model to the medically important arbovirus Ross River virus (RRV), in Brisbane, Australia. We found that vertebrate species with high physiological competence werent the most important for community transmission. Instead, we estimated that humans (previously overlooked as epidemiologically important hosts) potentially play an important role in RRV transmission, in part, because highly competent vectors readily feed on them and are highly abundant. By contrast, vectors with high physiological competence were also important for community transmission. Finally, we uncovered two potential transmission cycles: an enzootic cycle involving birds and an urban cycle involving humans. This modelling approach has direct application to other zoonotic arboviruses.

ecology↗

Historical and contemporary signatures of selection in response to transmissible cancer in the Tasmanian Devil (Sarcophilus harrisii)

Tasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. Here we compared signatures of selection across temporal scales to determine whether genes or gene pathways under contemporary selection (6-8 generations) have also been subject to historical selection (65-85 million years), and test for recurrent selection in devils. First, we used a targeted sequencing approach, RAD-capture, to identify genomic regions subject to rapid evolution in approximately 2,500 devils in six populations as DFTD spread across the species range. We documented genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. Then we used a molecular evolution approach to identify historical positive selection in devils compared to other marsupials and found evidence of selection in 1,773 genes. However, we found limited overlap across time scales, with historical selection detected in only 16 contemporary candidate genes, and no overlap in enriched functional gene sets. Our results are consistent with a novel, multi-locus evolutionary response of devils to DFTD. Our results can inform management actions to conserve adaptive potential of devils by identifying high priority targets for genetic monitoring and maintenance of functional diversity in managed populations.

evolutionary biology↗

Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors such as disease. The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a nearly 100% fatal, transmissible cancer, devil facial tumor disease (DFTD). Devils persist in regions of long-term infection despite epidemiological model predictions of species extinction, suggesting possible adaptation to DFTD. Here, we test the extent to which spatial variation and genetic diversity are associated with the abiotic environment and/or by DFTD. We employ genetic-environment association (GEAs) analyses using a RAD-capture panel consisting of 6,886 SNPs from 3,286 individuals sampled pre- and post-disease arrival. Pre-disease, we find significant correlations of allele frequencies with environmental variables, including 349 unique loci linked to 64 genes, suggesting local adaptation to abiotic environment. Following DFTD arrival, however, we detected few of the pre-disease candidate loci, but instead frequencies of candidate loci linked to 14 genes correlated with disease prevalence. Loss of apparent signal of abiotic local adaptation following disease arrival suggests swamping by the strong selection imposed by DFTD. Further support for this result comes from the fact that post-disease candidate loci are in linkage disequilibrium with genes putatively involved in immune response, tumor suppression and apoptosis. This suggests the strength GEA associations of loci with the abiotic environment are swamped resulting from the rapid onset of a biotic selective pressure.

evolutionary biology↗

Relation of seasonal birth pulses and maternal immunity with viral invasion and persistence: A case study of Hendra virus infection in a population of black flying foxes (Pteropus alecto)

Increasing outbreaks of emerging infectious diseases, originating from wildlife, has intensified interest in understanding the dynamics of these diseases in their wildlife reservoir hosts. Until recently, the effect of seasonal birth pulses and subsequent waning of maternally derived antibodies on epidemics in a wild mammal population has received little attention and has remained obscure. In this study, we explore how population structure, influenced by seasonal breeding and maternally derived immunity, affects viral invasion and persistence, using a hypothetical system loosely based on Hendra virus infection in black flying foxes (Pteropus alecto). We used deterministic epidemic models to simulate transient epidemics, following viral introduction into an infection-free population, with a variety of timings within a year and different levels of pre-existing herd immunity. Moreover, we applied different levels of birth synchrony and different modelling methods of waning maternal immunity to examine the effect of birth pulses and maternally derived immunity, both individually and in combination. The presence of waning maternal immunity dispersed the supply time of susceptible individuals in seasonally breeding populations, hence diminishing the effect of birth pulse. Dampened epidemics, caused by waning maternal immunity, made viral invasion and persistence easier. This study enhanced our understanding of viral invasion, persistence, and timing of epidemics in wildlife populations.

epidemiology↗

Interpreting mosquito feeding patterns in Australia through an ecological lens; an analysis of blood meal studies.

Mosquito-borne pathogens contribute significantly to the global burden of disease, infecting millions of people each year. Mosquito feeding is critical to the transmission dynamics of pathogens, and thus it is important to understanding and interpreting mosquito feeding patterns. In this paper we explore mosquito feeding patterns and their implications for disease ecology through a meta-analysis of published blood meal results collected across Australia from more than 12,000 blood meals from 22 species. To assess mosquito-vertebrate associations and identify mosquitoes on a spectrum of generalist or specialist feeders, we analysed blood meal data in two ways; first using a novel odds ratio analysis, and secondly by calculating Shannon diversity scores. We find that each mosquito species had a unique feeding association with different vertebrates, suggesting species-specific feeding patterns. Broadly, mosquito species could be grouped broadly into those that were primarily ornithophilic and those that fed more often on livestock. Aggregated feeding patterns observed across Australia were not explained by intrinsic variables such as mosquito genetics or larval habitats. We discuss the implications for disease transmission by vector mosquito species classified as generalist-feeders (such as Aedes vigilax and Culex annulirostris), or specialists (such as Aedes aegypti) in light of potential influences on mosquito host choice. Overall, we find that whilst existing blood meal studies in Australia are useful for investigating mosquito feeding patterns, standardisation of blood meal study methodologies and analyses, including the incorporation of vertebrate surveys, would improve predictions of the impact of vector-host interactions on disease ecology. Our analysis can also be used as a framework to explore mosquito-vertebrate associations, in which host availability data is unavailable, in other global systems.

ecology↗

Optimizing non-invasive sampling of an infectious bat virus

Notable outbreaks of infectious viruses resulting from spillover events from bats have brought much attention to the ecological origins of bat-borne zoonoses, resulting in an increase in ecological and epidemiological studies on bat populations in Africa, Asia, and Australia. The aim of many of these studies is to identify new viral agents with field sampling methods that collect pooled urine samples from large plastic sheets placed under a bat roost. The efficiency of under-roost sampling also makes it an attractive method for gathering roost-level prevalence data. However, the method allows multiple individuals to contribute to a pooled sample, potentially introducing positive bias. To assess the ability of under-roost sampling to accurately estimate viral prevalence, we constructed a probabilistic model to explore the relationship between four sampling designs (quadrant, uniform, stratified, and random) and estimation bias. We modeled bat density and movement with a Poisson cluster process and spatial kernels, and simulated the four underroost sheet sampling designs by manipulating a spatial grid of hexagonal tiles. We performed global sensitivity analyses to identify major sources of estimation bias and provide recommendations for field studies that wish to estimate roost-level prevalence. We found that the quadrant-based design had a positive bias 5-7 times higher than other designs due to spatial auto-correlation among sampling sheets and clustering of bats in the roost. The sampling technique is therefore highly sensitive to viral presence; but lacks specificity, providing poor information regarding dynamics in viral prevalence. Given population sizes of 5000-14000, our simulation results indicate that using a stratified random design to collect 30-40 urine samples from 80-100 sheets, each with an area of 0.75-1m2, would provide sufficient estimation of true prevalence with minimum sampling bias and false negatives. However, acknowledging the general problem of data aggregation, we emphasize that robust inference of true prevalence from field data require information of underpinning roost sizes. Our findings refine our understanding of the underroost sampling technique with the aim of increasing its specificity, and suggest that the method be further developed as an efficient non-invasive sampling technique that provides roost-level estimates of viral prevalence within a bat population.

ecology↗