Sex-biased infections scale to population impacts for an emerging wildlife disease

Kailing, Macy J.; Hoyt, Joseph R.; White, J. Paul; Kaarakka, Heather M.; Redell, Jennifer A.; Leon, Ariel E; Rocke, Tonie E.; DePue, John E.; Scullon, William H.; Parise, Katy L.; Foster, Jeffrey T.; Kilpatrick, A. Marm; Langwig, Kate E.

doi:10.1098/rspb.2023.0040

Cited by 7 publications

(4 citation statements)

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“…Males and females differ in their genetics, physiology and behaviour-all of which can alter the likelihood and severity of infection [1][2][3][4][5][6] and the spread of pathogens [7][8][9][10][11][12]. Many attempts to define whether males or females are more likely to be damaged by a pathogen and become the 'sicker sex' have centred on host susceptibility (i.e.…”

Section: Introductionmentioning

confidence: 99%

“…the likelihood of infection at exposure), as this is the stage when pathogen encounter and sex differences in immunity first collide [13][14][15]. While in some taxa males appear to be more susceptible to infection [1,[16][17][18][19][20], there are many examples where it is females instead [12,[21][22][23][24]. Thus, while sex differences in susceptibility are widespread, attempts to identify the consistently 'sicker' sex have proven challenging [3].…”

Section: Introductionmentioning

confidence: 99%

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Is there a sicker sex? Dose relationships modify male–female differences in infection prevalence

Butterworth,

Heffernan,

Hall

2024

Proc. R. Soc. B.

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Throughout the animal kingdom, there are striking differences in the propensity of one sex or the other to become infected. However, precisely when we should expect males or females to be the sicker sex remains unclear. A major barrier to answering this question is that very few studies have considered how the susceptibility of males and females changes across the full range of pathogen doses encountered in nature. Without quantifying this ‘dose–susceptibility’ relationship, we have likely underestimated the scope for sex differences to arise. Here, we use the Daphnia magnia – Pasteuria ramosa system to reveal that sex differences in susceptibility are entirely dose-dependent, with pathogens having a higher probability of successfully establishing an infection in mature males at low doses, but mature females at high doses. The scope for male–female differences to emerge is therefore much greater than previously appreciated—extending to sex differences in the upper limits to infection success, per-propagule infectivity risks and density-dependent pathogen behaviour. Applying this expanded scope across the animal kingdom will help us understand when and why a sicker sex emerges, and the implications for diseases in nature—where sex ratios, age structure and pathogen densities vary drastically.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Is there a sicker sex? Dose relationships modify male–female differences in infection prevalence

Butterworth,

Heffernan,

Hall

2024

Proc. R. Soc. B.

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“…Males and females differ in their behaviour, physiology, and genetics -all of which can alter the likelihood and outcomes of infection (Poulin 1996;Zuk and McKean 1996;Sheridan et al 2000;Zuk 2009;Gipson and Hall 2016) and the dynamics of disease (Ferrari et al 2003;Cousineau and Alizon 2014;Úbeda and Jansen 2016;Hall and Mideo 2018;Rogers et al 2022;Kailing et al 2023). Of all processes, we may expect these sex differences to manifest most consistently in host susceptibility (i.e., the likelihood of infection at exposure), as this is the stage where pathogen encounter and sex differences in immunity first collide (Nunn et al 2009;Nhamoyebonde and Leslie 2014;Giefing-Kröll et al 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Of all processes, we may expect these sex differences to manifest most consistently in host susceptibility (i.e., the likelihood of infection at exposure), as this is the stage where pathogen encounter and sex differences in immunity first collide (Nunn et al 2009;Nhamoyebonde and Leslie 2014;Giefing-Kröll et al 2015). However, the more susceptible sex is in fact highly variable (Sheridan et al 2000;Kelly et al 2018) -while in some taxa males seem more susceptible to infection (Poulin 1996;Gray 1998;Adamo et al 2001;Morton and García-del-Pino 2013;Keiser et al 2020;Rosso et al 2020), there are many examples where it is females instead (Seeman and Nahrung 2004;Hillegass et al 2008;Sanchez et al 2011;Kailing et al 2023). Thus, while sex differences in susceptibility appear to be widespread, attempts to identify the consistently 'sicker' sex have proven challenging (Sheridan et al 2000;Kelly et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Is there a sicker sex? Dose relationships modify male-female differences in infection prevalence

Butterworth

Heffernan

Hall

2023

Preprint

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Throughout the animal kingdom there are striking differences in the propensity of one sex or the other to become infected. However, attempts to generalise when we should expect males or females to emerge as the sicker sex have proven challenging. We argue that this is because our current understanding of sex differences in susceptibility is inherently limited, as most inferences have come from field studies (where exposure dose is difficult to quantify), or by measuring infection rates in vitro at a limited range of pathogen doses. Without considering how susceptibility changes across a range of pathogen doses (i.e., the dose-susceptibility relationship), we have likely underestimated the scope in which sex differences can arise, reducing our capacity to accurately characterise the sicker sex. Here, to expand our scope, we use the Daphnia magnia and Pasteuria ramosa system to measure infection prevalence across a fifteen thousandfold change in pathogen dose and quantify male and female differences through formal models of environmental transmission. Through this, we reveal that the expression of sex differences in susceptibility is entirely dose-dependent, with males more susceptible at low doses, and females more susceptible at high doses. The scope for male-female differences to emerge is therefore much greater than previously expected - extending to differences in absolute resistance, per-propagule infectivity risks, and the dose-specific behaviour of pathogens. Crucially, none of these components in isolation could define the sicker sex. If we wish to understand the broader patterns underlying whether males or females are the sicker sex, there is a need to apply this expanded scope across the animal kingdom. This will help us understand when and why a sicker sex emerges, and the implications for diseases in nature - where sex ratios and pathogen densities vary drastically.

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Capture rates of Eptesicus fuscus increase following white‐nose syndrome across the eastern US

Simonis,

Hartzler,

Turner

et al. 2024

Ecology and Evolution

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Emerging infectious diseases threaten wildlife globally. While the effects of infectious diseases on hosts with severe infections and high mortality rates often receive considerable attention, effects on hosts that persist despite infection are less frequently studied. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a persisting species susceptible to infection by the invasive fungal pathogen Pseudogymnoascus destructans (Pd; causative agent for white‐nose syndrome), across the eastern US using a 30‐year dataset. Capture rates of male and female E. fuscus increased from preinvasion to pathogen establishment years, with greater increases to the capture rates of females than males. Among females, capture rates of pregnant and post‐lactating females increased by pathogen establishment. We outline potential mechanisms for these broad demographic changes in E. fuscus capture rates (i.e., increases to foraging from energy deficits created by Pd infection, increases to relative abundance, or changes to reproductive cycles), and suggest future research for identifying mechanisms for increasing capture rates across the eastern US. These data highlight the importance of understanding how populations of persisting host species change following pathogen invasion across a broad spatial scale. Understanding changes to population composition following pathogen invasion can identify broad ecological patterns across space and time, and open new avenues for research to identify drivers of those patterns.

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Sex-biased infections scale to population impacts for an emerging wildlife disease

Cited by 7 publications

References 100 publications

Is there a sicker sex? Dose relationships modify male–female differences in infection prevalence

Is there a sicker sex? Dose relationships modify male–female differences in infection prevalence

Is there a sicker sex? Dose relationships modify male-female differences in infection prevalence

Capture rates of Eptesicus fuscus increase following white‐nose syndrome across the eastern US

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