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Article ; Online: Multi-locus homozygosity promotes actuarial senescence in a wild mammal.

Hudson, Dave W / McKinley, Trevelyan J / Benton, Clare H / Delahay, Richard / McDonald, Robbie A / Hodgson, Dave J

2023 Volume 92, Issue 9, Page(s) 1881–1892

Abstract: Genome-wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will ...

Abstract	Genome-wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will filter out negative impacts on younger individuals with greater reproductive value. Here we infer associations between multi-locus homozygosity (MLH), sex, disease and age-dependent mortality risks using Bayesian analysis of the life histories of wild European badgers Meles meles in a population naturally infected with Mycobacterium bovis (the causative agent of bovine tuberculosis [bTB]). We find important effects of MLH on all parameters of the Gompertz-Makeham mortality hazard function, but particularly in later life. Our findings confirm the predicted association between genomic homozygosity and actuarial senescence. Increased homozygosity is particularly associated with an earlier onset, and greater rates of actuarial senescence, regardless of sex. The association between homozygosity and actuarial senescence is further amplified among badgers putatively infected with bTB. These results recommend further investigation into the ecological and behavioural processes that result in genome-wide homozygosity, and focused work on whether homozygosity is harmful or beneficial during early life-stages.
MeSH term(s)	Animals ; Cattle ; Bayes Theorem ; Mycobacterium bovis ; Tuberculosis, Bovine/epidemiology ; Mustelidae ; Cattle Diseases
Language	English
Publishing date	2023-07-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.13979
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Article ; Online: Multi‐locus homozygosity promotes actuarial senescence in a wild mammal

Hudson, Dave W. / McKinley, Trevelyan J. / Benton, Clare H. / Delahay, Richard / McDonald, Robbie A. / Hodgson, Dave J.

Journal of Animal Ecology. 2023 Sept., v. 92, no. 9 p.1881-1892

2023

Abstract: Genome‐wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will ...

Abstract	Genome‐wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will filter out negative impacts on younger individuals with greater reproductive value. Here we infer associations between multi‐locus homozygosity (MLH), sex, disease and age‐dependent mortality risks using Bayesian analysis of the life histories of wild European badgers Meles meles in a population naturally infected with Mycobacterium bovis (the causative agent of bovine tuberculosis [bTB]). We find important effects of MLH on all parameters of the Gompertz–Makeham mortality hazard function, but particularly in later life. Our findings confirm the predicted association between genomic homozygosity and actuarial senescence. Increased homozygosity is particularly associated with an earlier onset, and greater rates of actuarial senescence, regardless of sex. The association between homozygosity and actuarial senescence is further amplified among badgers putatively infected with bTB. These results recommend further investigation into the ecological and behavioural processes that result in genome‐wide homozygosity, and focused work on whether homozygosity is harmful or beneficial during early life‐stages.
Keywords	Bayesian theory ; Meles meles ; Mycobacterium bovis ; animal ecology ; bovine tuberculosis ; etiological agents ; genomics ; homozygosity ; mammals ; mortality ; natural selection ; reproduction
Language	English
Dates of publication	2023-09
Size	p. 1881-1892.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.13979
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Identifying likely transmissions in Mycobacterium bovis infected populations of cattle and badgers using the Kolmogorov Forward Equations.

Rossi, Gianluigi / Crispell, Joseph / Balaz, Daniel / Lycett, Samantha J / Benton, Clare H / Delahay, Richard J / Kao, Rowland R

Scientific reports

2020 Volume 10, Issue 1, Page(s) 21980

Abstract: Established methods for whole-genome-sequencing (WGS) technology allow for the detection of single-nucleotide polymorphisms (SNPs) in the pathogen genomes sourced from host samples. The information obtained can be used to track the pathogen's evolution ... ...

Abstract	Established methods for whole-genome-sequencing (WGS) technology allow for the detection of single-nucleotide polymorphisms (SNPs) in the pathogen genomes sourced from host samples. The information obtained can be used to track the pathogen's evolution in time and potentially identify 'who-infected-whom' with unprecedented accuracy. Successful methods include 'phylodynamic approaches' that integrate evolutionary and epidemiological data. However, they are typically computationally intensive, require extensive data, and are best applied when there is a strong molecular clock signal and substantial pathogen diversity. To determine how much transmission information can be inferred when pathogen genetic diversity is low and metadata limited, we propose an analytical approach that combines pathogen WGS data and sampling times from infected hosts. It accounts for 'between-scale' processes, in particular within-host pathogen evolution and between-host transmission. We applied this to a well-characterised population with an endemic Mycobacterium bovis (the causative agent of bovine/zoonotic tuberculosis, bTB) infection. Our results show that, even with such limited data and low diversity, the computation of the transmission probability between host pairs can help discriminate between likely and unlikely infection pathways and therefore help to identify potential transmission networks. However, the method can be sensitive to assumptions about within-host evolution.
MeSH term(s)	Animals ; Cattle/microbiology ; Models, Biological ; Mustelidae/microbiology ; Mycobacterium bovis/physiology ; Probability ; Tuberculosis/epidemiology ; Tuberculosis/microbiology ; Tuberculosis/transmission ; Tuberculosis/veterinary
Language	English
Publishing date	2020-12-15
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-78900-3
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Article: What has molecular epidemiology ever done for wildlife disease research? Past contributions and future directions

Benton, Clare H / Delahay, Richard J / Trewby, Hannah / Hodgson, David J

European journal of wildlife research. 2015 Feb., v. 61, no. 1

2015

Abstract: The increasing availability of novel molecular techniques has transformed the study of human health and disease epidemiology. However, uptake of such approaches has been more conservative in the field of wildlife disease epidemiology. We consider the ... ...

Abstract	The increasing availability of novel molecular techniques has transformed the study of human health and disease epidemiology. However, uptake of such approaches has been more conservative in the field of wildlife disease epidemiology. We consider the reasons for this and discuss current and potential applications of molecular techniques in a variety of relevant areas within the field of wildlife disease research. These include conducting wildlife disease surveillance, identifying sources of pathogen emergence, uncovering host-pathogen dynamics and managing current outbreaks, including the development and monitoring of wildlife vaccines. We highlight key examples of applications of molecular epidemiological approaches to wildlife disease scenarios and draw parallels from human disease research to suggest potential future directions. The potential value of next generation sequencing technologies to the field of wildlife disease research is discussed, and initial applications are highlighted, balanced against consideration of the challenges involved. Using a wide range of examples drawn from research into human, livestock and wildlife diseases, we demonstrate the value of using molecular epidemiological approaches at all scales of wildlife disease research, from pathogen strains circulating at a global scale to intra-individual host-pathogen dynamics. The potential future contribution of these technologies to the field of wildlife disease epidemiology is substantial. In particular, they are likely to play an increasingly important role in helping us to address a principal challenge in the management of wildlife diseases which is how to tease apart the transmission dynamics of complex multi-host systems in order to develop effective and sustainable interventions.
Keywords	disease surveillance ; high-throughput nucleotide sequencing ; human diseases ; human health ; humans ; livestock ; molecular epidemiology ; pathogens ; vaccines ; wildlife ; wildlife diseases ; wildlife management
Language	English
Dates of publication	2015-02
Size	p. 1-16.
Publishing place	Springer-Verlag
Document type	Article
ZDB-ID	2141660-6
ISSN	1439-0574 ; 1612-4642
ISSN (online)	1439-0574
ISSN	1612-4642
DOI	10.1007/s10344-014-0882-4
Database	NAL-Catalogue (AGRICOLA)

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Article: Inbreeding intensifies sex‐ and age‐dependent disease in a wild mammal

Benton, Clare H / Andrew J. Young / Andrew Robertson / Dave Hodgson / Freya A. P. Smith / Richard J. Delahay / Robbie A. McDonald / Terry A. Burke

journal of animal ecology. 2018 Nov., v. 87, no. 6

2018

Abstract: The mutation accumulation theory of senescence predicts that age‐related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and ... ...

Abstract	The mutation accumulation theory of senescence predicts that age‐related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long‐term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age‐related increase in the impact of inbreeding on a fitness‐relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late‐life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age‐dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late‐life declines in components of fitness that characterise senescence. Better understanding of sex‐specific links between inbreeding, disease and ageing provides insights into population‐level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
Keywords	alleles ; antibodies ; badgers ; bovine tuberculosis ; females ; homozygosity ; inbreeding ; inbreeding depression ; males ; Meles meles ; mutation accumulation ; pathogens ; prediction ; wildlife ; wildlife diseases ; zoonoses
Language	English
Dates of publication	2018-11
Size	p. 1500-1511.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.12878
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal.

Benton, Clare H / Delahay, Richard J / Robertson, Andrew / McDonald, Robbie A / Wilson, Alastair J / Burke, Terry A / Hodgson, Dave

Proceedings. Biological sciences

2016 Volume 283, Issue 1835

Abstract: The importance of social- and kin-structuring of populations for the transmission of wildlife disease is widely assumed but poorly described. Social structure can help dilute risks of transmission for group members, and is relatively easy to measure, but ...

Abstract	The importance of social- and kin-structuring of populations for the transmission of wildlife disease is widely assumed but poorly described. Social structure can help dilute risks of transmission for group members, and is relatively easy to measure, but kin-association represents a further level of population sub-structure that is harder to measure, particularly when association behaviours happen underground. Here, using epidemiological and molecular genetic data from a wild, high-density population of the European badger (Meles meles), we quantify the risks of infection with Mycobacterium bovis (the causative agent of tuberculosis) in cubs. The risk declines with increasing size of its social group, but this net dilution effect conceals divergent patterns of infection risk. Cubs only enjoy reduced risk when social groups have a higher proportion of test-negative individuals. Cubs suffer higher infection risk in social groups containing resident infectious adults, and these risks are exaggerated when cubs and infectious adults are closely related. We further identify key differences in infection risk associated with resident infectious males and females. We link our results to parent-offspring interactions and other kin-biased association, but also consider the possibility that susceptibility to infection is heritable. These patterns of infection risk help to explain the observation of a herd immunity effect in badgers following low-intensity vaccination campaigns. They also reveal kinship and kin-association to be important, and often hidden, drivers of disease transmission in social mammals.
MeSH term(s)	Animals ; Behavior, Animal ; Female ; Male ; Mustelidae/microbiology ; Mycobacterium bovis ; Population Density ; Prevalence ; Social Behavior ; Tuberculosis/transmission
Language	English
Publishing date	2016-07-21
Publishing country	England
Document type	Journal Article
ZDB-ID	209242-6
ISSN	1471-2954 ; 0080-4649 ; 0962-8452 ; 0950-1193
ISSN (online)	1471-2954
ISSN	0080-4649 ; 0962-8452 ; 0950-1193
DOI	10.1098/rspb.2016.0798
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Article ; Online: (with research data) Inbreeding intensifies sex- and age-dependent disease in a wild mammal.

Benton, Clare H / Delahay, Richard J / Smith, Freya A P / Robertson, Andrew / McDonald, Robbie A / Young, Andrew J / Burke, Terry A / Hodgson, Dave

The Journal of animal ecology

2018 Volume 87, Issue 6, Page(s) 1500–1511

Abstract: The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and ... ...

Abstract	The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
MeSH term(s)	Animals ; Cattle ; Female ; Inbreeding ; Inbreeding Depression ; Male ; Mustelidae ; Population Dynamics ; Tuberculosis, Bovine
Language	English
Publishing date	2018-07-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.12878
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Combining genomics and epidemiology to analyse bi-directional transmission of

Crispell, Joseph / Benton, Clare H / Balaz, Daniel / De Maio, Nicola / Ahkmetova, Assel / Allen, Adrian / Biek, Roman / Presho, Eleanor L / Dale, James / Hewinson, Glyn / Lycett, Samantha J / Nunez-Garcia, Javier / Skuce, Robin A / Trewby, Hannah / Wilson, Daniel J / Zadoks, Ruth N / Delahay, Richard J / Kao, Rowland Raymond

eLife

2019 Volume 8

Abstract: Quantifying pathogen transmission in multi-host systems is difficult, as exemplified in bovine tuberculosis (bTB) systems, but is crucial for control. The agent of bTB, ...

Abstract	Quantifying pathogen transmission in multi-host systems is difficult, as exemplified in bovine tuberculosis (bTB) systems, but is crucial for control. The agent of bTB,
MeSH term(s)	Animals ; Animals, Wild/microbiology ; Bayes Theorem ; Cattle ; Disease Reservoirs/microbiology ; Genome, Bacterial/genetics ; Genomics/methods ; Host-Pathogen Interactions ; Mustelidae/microbiology ; Mycobacterium bovis/classification ; Mycobacterium bovis/genetics ; Mycobacterium bovis/physiology ; Phylogeny ; Tuberculosis, Bovine/epidemiology ; Tuberculosis, Bovine/microbiology ; Tuberculosis, Bovine/transmission
Language	English
Publishing date	2019-12-17
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.45833
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: What has molecular epidemiology ever done for wildlife disease research? Past contributions and future directions

Benton, Clare H. / Delahay, Richard J. / Trewby, Hannah / Hodgson, David J.

European journal of wildlife research

Volume v. 61,, Issue no. 1

Abstract	The increasing availability of novel molecular techniques has transformed the study of human health and disease epidemiology. However, uptake of such approaches has been more conservative in the field of wildlife disease epidemiology. We consider the reasons for this and discuss current and potential applications of molecular techniques in a variety of relevant areas within the field of wildlife disease research. These include conducting wildlife disease surveillance, identifying sources of pathogen emergence, uncovering host-pathogen dynamics and managing current outbreaks, including the development and monitoring of wildlife vaccines. We highlight key examples of applications of molecular epidemiological approaches to wildlife disease scenarios and draw parallels from human disease research to suggest potential future directions. The potential value of next generation sequencing technologies to the field of wildlife disease research is discussed, and initial applications are highlighted, balanced against consideration of the challenges involved. Using a wide range of examples drawn from research into human, livestock and wildlife diseases, we demonstrate the value of using molecular epidemiological approaches at all scales of wildlife disease research, from pathogen strains circulating at a global scale to intra-individual host-pathogen dynamics. The potential future contribution of these technologies to the field of wildlife disease epidemiology is substantial. In particular, they are likely to play an increasingly important role in helping us to address a principal challenge in the management of wildlife diseases which is how to tease apart the transmission dynamics of complex multi-host systems in order to develop effective and sustainable interventions.
Keywords	human health ; disease surveillance ; vaccines ; wildlife diseases ; human diseases ; wildlife management ; wildlife ; molecular epidemiology ; humans ; pathogens ; livestock ; high-throughput nucleotide sequencing
Language	English
Document type	Article
ISSN	1612-4642
Database	AGRIS - International Information System for the Agricultural Sciences and Technology

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