Interpopulation differences in male reproductive effort drive the population dynamics of a host exposed to an emerging fungal pathogen

Abstract

Compensatory recruitment is a key demographic mechanism that has allowed the coexistence of populations of susceptible amphibians with Batrachochytrium dendrobatidis (Bd), a fungus causing one of the most devastating emerging infectious disease ever recorded among vertebrates. However, the underlying processes (e.g. density‐dependent increase in survival at early life stages, change in reproductive traits) as well as the level of interpopulation variation in this response are poorly known. We explore potential mechanisms of compensatory recruitment in response to Bd infection by taking advantage of an amphibian system where male reproductive traits are easy to quantify in free‐living populations. The Southern Darwin's frog Rhinoderma darwinii is a vocal sac‐brooding species that exhibits a high susceptibility to lethal Bd infection. Using a 7‐year capture–recapture study at four populations with contrasting Bd infection status (one high prevalence, one low prevalence and two Bd‐free populations), we evaluated whether Bd‐positive populations exhibited a higher adult recruitment and a higher male reproductive effort than Bd‐negative populations. We also estimated population growth rates to explore whether recruitment compensated for the negative impacts of Bd on the survival of adults. In addition, we evaluated a potential demographic signal of compensatory recruitment (i.e. positive relationship between the proportion of juveniles and Bd prevalence) in response to Bd infection using raw count data from 13 R. darwinii populations. The high Bd prevalence population exhibited the highest male reproductive effort and the highest recruitment among the four monitored populations. This led to a growing population during the study period despite high mortality of adult hosts. In contrast, males from the population with low Bd prevalence had a low reproductive effort and this population, which had the lowest adult recruitment, was declining during the study period despite adults having a higher survival in comparison to the high Bd prevalence population. We also found a demographic signal of compensatory recruitment in response to Bd infection in our broader analysis of 13 R. darwinii populations. Our study underlines the importance of interpopulation variation in life‐history strategies on the fate of host populations after infectious disease emergence. Our results also suggest that an increase in reproductive effort can be one of the processes underlying compensatory recruitment in populations of Bd‐susceptible amphibians.

Context‐dependent variation in persistence of host populations in the face of disease

“…Fecundity compensation (Minchella & Loverde, 1981) is the process whereby hosts respond to high disease-induced mortality by increasing reproductive effort. Valenzuela-Sánchez et al (2022) propose that this response could arise through three pathways: (a) density dependence, (b) pathogen-induced adaptive plasticity via trade-offs or (c) rapid evolutionary change (Figure 1) and provide their arguments as to which is most likely. The authors suggest that density dependence (pathway 1) is an unlikely mechanism as both Bd-positive populations had similarly low densities, but only the high Bd-prevalence population showed evidence of compensatory recruitment.…”

“…The study by Valenzuela-Sánchez et al (2022) provides quantitative evidence of interpopulation variation in response to emerging infectious disease and highlights the importance of capturing this variation. When approaching problems in large multi-host disease systems, there may be few tenets that hold true across all species and populations, a situation that is somewhat double-edged.…”

“…However, despite the large body of literature that provides support for compensatory recruitment as a driver of population persistence in amphibian species affected by the amphibian chytrid fungus (Lampo et al, 2017;Muths et al, 2011;Phillott et al, 2013;Scheele et al, 2015;Tobler et al, 2012;West et al, 2020) (Batrachochytrium dendrobatidis; Bd), there has been no investigation of the exact pathways that generate this response until the study highlighted here (Valenzuela-Sánchez et al, 2022). In what is arguably the most devastating wildlife disease ever documented (Scheele et al, 2019), the increasing concern and need for strategies to mitigate amphibian decline make this paper (Valenzuela-Sánchez et al, 2022) particularly timely and important.…”

“…To infer the influence of life-history variation on population trajectories,Valenzuela-Sánchez et al (2022) used generation time, calculated from their population matrix model, as a proxy to place focal populations on the slow-fast continuum. Their results indicated that the high Bd-prevalence population and one Bd-negative population had short generation times, which they equated with having fast life histories.…”

“…In contrast, the low Bd-prevalence population and the other Bd-negative population had long generation times, placing them with slow life histories. Therefore, the differences in demographic response to disease between the two Bd-positive populations could be due to the selective pressure of Bd (high vs. low prevalence), a naturally slow or fast life history regardless of Bd, or a combination of both Valenzuela-Sánchez et al (2022). argue that because the generation time of the fast-living, high Bd-prevalence population is 5x higher than the fast-living, Bd-negative population, that the observed compensatory recruitment response can likely be attributed to the presence of Bd and this scenario presents a framework for future study.…”