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Life history and population regulation shape demographic competence and influence the maintenance of endemic disease

Abstract

Host life history and demography play important roles in host–pathogen dynamics, by influencing the ability of hosts and their pathogens to coexist. We introduce the concept of demographic competence to describe the ability of host populations to sustain endemic infectious disease. Hosts with high demographic competence are more likely to act as keystone hosts and constitute reservoirs of infection that can spill over into other species. We propose that the pace of host life history will interact with pathogen life history to influence demographic competence. Our models demonstrate that slow-living hosts (with high survival and low recruitment rates) have greater demographic competence than fast-living hosts (with low survival and high recruitment rates) for susceptible–infected disease dynamics, although this difference is reduced when populations of slow hosts are age structured. Demographic competence is generally greater among hosts with populations regulated by survival compared to reproduction, but this difference is smallest among slow life histories and reversed for some pathogens with frequency-dependent transmission. An association between pathogen life history traits and the demographic competence of faster-living hosts also has implications for trade-offs between pathogen virulence and transmissibility. Overall, we demonstrate how host life history traits can help predict wildlife reservoirs of zoonoses and the vulnerability of populations to disease-induced extinction.

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Fig. 1: Demographic competence as a function of host population size and pathogen prevalence.
Fig. 2: The relationship between host pace of life and demographic competence for pathogens with DD transmission when host population regulation is based on either survival or reproduction.
Fig. 3: The difference in demographic competence between host populations with survival- and reproduction-based regulation for hosts with different paces of life and pathogens with DD transmission.
Fig. 4: The relationship between host pace of life and demographic competence for pathogens with FD transmission when host population regulation is based on either survival or reproduction.
Fig. 5: The impact of host pace of life on the relative importance of reproduction- versus survival-based population regulation in generating demographically competent host populations for a pathogen with FD transmission across a range of strengths of host population regulation.

Data availability

No empirical data were used in this study. All data and plots can be generated using the computer code provided.

Code availability

Code for running the models and plotting the output are provided in the Supplementary Information and are available at https://github.com/matthewsilk/DemographicCompetence.

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Acknowledgements

M.J.S. is funded by the University of Exeter.

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D.J.H. and M.J.S. both developed the idea for the work. M.J.S. developed the models based on code provided by D.J.H. Both authors drafted and revised the manuscript.

Corresponding authors

Correspondence to Matthew J. Silk or David J. Hodgson.

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Extended data

Extended Data Fig. 1 The impact of host pace-of-life (columns, slower as you move right) on the relative importance of reproduction-based versus survival-based host population regulation in generating demographically competent host populations for a pathogen with density-dependent transmission across a range of strengths of host population regulation (rows, increasing as you go up).

The y axis of each panel represents pathogen transmissibility and the x axis represents pathogen virulence (in terms of its effect on host mortality). Dark blue represents survival-based regulation producing much higher demographic competence. Bright green represents reproduction-based regulation producing much higher demographic competence. White represents density-dependent survival and reproduction producing a similar effect. Grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of pathogen extinction.

Extended Data Fig. 2 The relationship between host pace-of-life and demographic competence for population with age structure, pathogens with DD transmission and when either host population regulation is survival-based (red) or reproduction-based (blue).

Demographic competence is pathogen prevalence multiplied by the host population size relative to the uninfected carrying capacity. We show results from models that consider hosts as either susceptible or infected (see above) for two different values for juvenile survival. Closed circles and solid lines represent juvenile survival being equal to adult survival and open circles and dashed lines represent juvenile survival being 60% of adult survival. The comparable values for populations without age structure are indicated by crosses (red for survival-based regulation and blue for reproduction-based regulation).

Extended Data Fig. 3 The difference in demographic competence between host populations with survival-based and reproduction-based regulation for age-structured host populations with intermediate or slow pace-of-life when pathogens transmission is density-dependent.

Here we depict the effect of pathogen virulence (x axis) on the demographic competence of host populations with survival-based regulation minus the demographic competence of host populations with reproduction-based regulation (y axis) for the case when juvenile survival is equal to adult survival. This is done for three different transmission rates (red: high, orange: intermediate and yellow: low), for three different host paces-of-life, and for strong and weak host population regulation (rows). A difference of zero will typically indicate neither host population being able to maintain the pathogen.

Extended Data Fig. 4 The impact of host pace-of-life (columns, slower as you move right) on the relative importance of reproduction-based versus survival-based host population regulation for demographic competence of an age structured population in which juvenile survival is equal to adult survival; this figure shows results for a pathogen with density-dependent transmission across a range of intensities of host population regulation (rows, increasing as you go up).

The y axis of each panel represents pathogen transmissibility and the x axis represents pathogen virulence (in terms of its effect on host mortality). Dark blue represents survival-based regulation producing much higher demographic competence. Bright green represents reproduction-based regulation producing much higher demographic competence. White represents survival-based and reproduction-based regulation producing a similar effect. Grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of pathogen extinction.

Extended Data Fig. 5 The impact of host pace-of-life (columns, slower as you move right) on the relative importance of reproduction-based versus survival-based host population regulation for demographic competence of an age structured population in which juvenile survival is less than adult survival; this figure shows results for a pathogen with density-dependent transmission across a range of intensities of host population regulation (rows, increasing as you go up).

The y axis of each panel represents pathogen transmissibility and the x axis represents pathogen virulence (in terms of its effect on host mortality). Dark blue represents survival-based regulation producing much higher demographic competence. Bright green represents reproduction-based regulation producing much higher demographic competence. White represents survival-based and reproduction-based regulation producing a similar effect. Grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of pathogen extinction.

Extended Data Fig. 6 The relationship between host pace-of-life and demographic competence for population with age structure, pathogens with FD transmission and when either host population regulation is survival-based (red) or reproduction-based (blue).

Demographic competence is pathogen prevalence multiplied by the host population size relative to the uninfected carrying capacity. We show results from models that consider hosts as either susceptible or infected (see above) for two different values for juvenile survival. Closed circles and solid lines represent juvenile survival being equal to adult survival and open circles and dashed lines represent juvenile survival being 60% of adult survival. The comparable values for populations without age structure are indicated by crosses (red for survival-based regulation and blue for reproduction-based regulation).

Extended Data Fig. 7 The impact of host pace-of-life (columns) on the relative importance of reproduction-based versus survival-based population regulation in generating demographically competent age-structured host populations in which juvenile survival is equal to adult survival; this figure shows results for a pathogen with frequency-dependent transmission across a range of strengths of host population regulation (rows, strength increasing from bottom to top).

The y axis of each panel represents pathogen transmissibility and the x axis represents pathogen virulence (in terms of its effect on host mortality). Dark blue represents survival-based regulation producing much higher demographic competence. Bright green represents reproduction-based regulation producing much higher demographic competence. White represents survival-based and reproduction-based regulation producing a similar effect. Grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of pathogen extinction. Dark grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of host extinction.

Extended Data Fig. 8 The impact of host pace-of-life (columns) on the relative importance of reproduction-based versus survival-based population regulation in generating demographically competent age-structured host populations in which juvenile survival is less than adult survival; this figure shows results for a pathogen with frequency-dependent transmission across a range of strengths of host population regulation (rows, strength increasing from bottom to top).

The y axis of each panel represents pathogen transmissibility and the x axis represents pathogen virulence (in terms of its effect on host mortality). Dark blue represents survival-based regulation producing much higher demographic competence. Bright green represents reproduction-based regulation producing much higher demographic competence. White represents survival-based and reproduction-based regulation producing a similar effect. Grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of pathogen extinction. Dark grey represents regions where neither reproduction-based nor survival-based regulation can maintain endemic disease in a starting population of 1000 hosts as a result of host extinction.

Supplementary information

Supplementary Information

Supplementary Notes 1–3 and Figs. 1–12.

Reporting Summary

Peer Review Information

Supplementary Software 1

Main code for DD transmission.

Supplementary Software 2

Main code for FD transmission.

Supplementary Software 3

Main plotting code.

Supplementary Software 4

Age structure code for DD transmission.

Supplementary Software 5

Age structure code for FD transmission.

Supplementary Software 6

Age structure plotting code.

Supplementary Software 7

Supplementary code for reordered life events (RIS): DD transmission.

Supplementary Software 8

Supplementary code for reordered life events (RIS): FD transmission.

Supplementary Software 9

Supplementary code for reordered life events (RSI): DD transmission.

Supplementary Software 10

Supplementary code for reordered life events (RSI): FD transmission.

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Silk, M.J., Hodgson, D.J. Life history and population regulation shape demographic competence and influence the maintenance of endemic disease. Nat Ecol Evol 5, 82–91 (2021). https://doi.org/10.1038/s41559-020-01333-8

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