Sustained Drought, but Not Short-Term Warming, Alters the Gut Microbiomes of Wild
            <i>Anolis</i>
            Lizards

Williams, Claire; Kueneman, Jordan G.; Nicholson, Daniel J.; Rosso, Adam A; Folfas, Edita; Casement, Brianna; Gallegos-Koyner, Maria A; Neel, Lauren K.; Curlis, John David; McMillan, W. Owen; Cox, Christian L.; Logan, Michael L.

doi:10.1128/aem.00530-22

Cited by 14 publications

(10 citation statements)

References 91 publications

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“…For example, in Pellerin et al [16], the impact of warming on life-history traits varied across years and could be explained by inter-annual variation in climate treatments or/and by lizards adaptation/acclimation to warming [49]. Our results further suggest that the climate effects become stronger in the long term, consistent with another study that showed that the gut microbiome of the slender anole is resilient to warming in the short term but affected in the long term [50]. Both observations highlight that climate effects may progressively settle in time and emphasize the importance of long-term experiments when studying the response of the gut microbiome under climate change.…”

Section: Discussionsupporting

confidence: 88%

Warming effects on lizard gut microbiome depend on habitat connectivity

Fromm,

Zinger,

Pellerin

et al. 2024

Proc. R. Soc. B.

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Climate warming and landscape fragmentation are both factors well known to threaten biodiversity and to generate species responses and adaptation. However, the impact of warming and fragmentation interplay on organismal responses remains largely under-explored, especially when it comes to gut symbionts, which may play a key role in essential host functions and traits by extending its functional and genetic repertoire. Here, we experimentally examined the combined effects of climate warming and habitat connectivity on the gut bacterial communities of the common lizard ( Zootoca vivipara ) over three years. While the strength of effects varied over the years, we found that a 2°C warmer climate decreases lizard gut microbiome diversity in isolated habitats. However, enabling connectivity among habitats with warmer and cooler climates offset or even reversed warming effects. The warming effects and the association between host dispersal behaviour and microbiome diversity appear to be a potential driver of this interplay. This study suggests that preserving habitat connectivity will play a key role in mitigating climate change impacts, including the diversity of the gut microbiome, and calls for more studies combining multiple anthropogenic stressors when predicting the persistence of species and communities through global changes.

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Section: Discussionsupporting

confidence: 88%

Warming effects on lizard gut microbiome depend on habitat connectivity

Fromm,

Zinger,

Pellerin

et al. 2024

Proc. R. Soc. B.

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“…This study provides the first evidence that climate change is altering gut microbiotas in a longitudinally monitored wildlife population. These findings are in line with cross-sectional studies that have also found support for climate-induced changes to gut microbiotas in wild polar bears and anoles (Watson et al, 2019;Williams et al, 2022), and experimental studies that demonstrate the direct link between temperature and the gut microbiota across taxonomically diverse hosts (Chevalier et al, 2015;Li et al, 2023;. A major goal for future research is to identify the proximate mechanisms underpinning the link between climate change and changes in gut microbiotas.…”

Section: Discussionsupporting

confidence: 84%

“…However, little is known about how climate change and pathogen dynamics interact to shape the gut microbiota, a diverse bacterial community that is crucial for host physiological homoeostasis, pathogen defence, and thermal tolerance (Alavi et al, 2020; Honda & Littman, 2016; Jaramillo & Castañeda, 2021). Recent evidence suggests that the gut microbiota is affected directly and indirectly by climate change (Greenspan et al, 2020; Sepulveda & Moeller, 2020; Watson et al, 2019; Williams et al, 2022). However, whether such responses are adaptive or maladaptive for animal hosts remains unclear, because longitudinal time‐series data that document gut microbial responses to climate change in natural populations, and the consequences for host fitness, are rare.…”

Section: Introductionmentioning

confidence: 99%

Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats

Risely

Müller‐Klein²,

Schmid³

et al. 2023

Global Change Biology

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Climate change and climate‐driven increases in infectious disease threaten wildlife populations globally. Gut microbial responses are predicted to either buffer or exacerbate the negative impacts of these twin pressures on host populations. However, examples that document how gut microbial communities respond to long‐term shifts in climate and associated disease risk, and the consequences for host survival, are rare. Over the past two decades, wild meerkats inhabiting the Kalahari have experienced rapidly rising temperatures, which is linked to the spread of tuberculosis (TB). We show that over the same period, the faecal microbiota of this population has become enriched in Bacteroidia and impoverished in lactic acid bacteria (LAB), a group of bacteria including Lactococcus and Lactobacillus that are considered gut mutualists. These shifts occurred within individuals yet were compounded over generations, and were better explained by mean maximum temperatures than mean rainfall over the previous year. Enriched Bacteroidia were additionally associated with TB exposure and disease, the dry season and poorer body condition, factors that were all directly linked to reduced future survival. Lastly, abundances of LAB taxa were independently and positively linked to future survival, while enriched taxa did not predict survival. Together, these results point towards extreme temperatures driving an expansion of a disease‐associated pathobiome and loss of beneficial taxa. Our study provides the first evidence from a longitudinally sampled population that climate change is restructuring wildlife gut microbiota, and that these changes may amplify the negative impacts of climate change through the loss of gut mutualists. While the plastic response of host‐associated microbiotas is key for host adaptation under normal environmental fluctuations, extreme temperature increases might lead to a breakdown of coevolved host–mutualist relationships.

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Section: Introductionmentioning

confidence: 99%

“…Microbiome-mediated plasticity may assist animals in acclimatizing or adapting to environmental change (11, 12). Since microbiomes are highly dynamic, they can change on a more rapid timescale than their animal hosts in response to environmental pressures (12–19). Gut microbiota, in particular, play many vital roles in host physiology (20–23), and environmental change may lead to an imbalance in the microbiome, which can have negative outcomes for hosts.…”

Section: Introductionmentioning

confidence: 99%

Environmental change drives multi-generational shifts in the gut microbiome that mirror changing animal fitness

Williams,

King

et al. 2023

Preprint

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Gut microbiomes can dramatically affect host health and fitness and can also be highly dynamic in response to changing environmental conditions. This intricate interplay between gut microbiota, environmental pressures, and host health necessitates accounting for all these variables when predicting the response of animals to a changing environment. These predictions are of broad concern but are highly relevant to conservation biology, and more specifically to populations transitioning from the wild to human care for the purposes of ex-situ breeding programs. Captivity can dramatically alter both host-associated microbial communities and host health, but the dynamics of how the host and microbiome transition between the wild and captive state--within and across generations--are not well described. Here, we evaluate the microbiome and host fitness metrics for Pacific pocket mice (Perognathus longimembris pacificus) during the establishment of an ex-situ conservation breeding program to characterize how pocket mice and their microbiomes respond to the environmental pressures of captivity across five generations. We found that the microbiome assumes a novel, stable conformation after two to three generations in captivity and that the patterns observed in the transitioning microbiota mirror the patterns of transitioning hosts' weight and reproductive metrics. Moreover, we identify several microbial taxa which are correlated with successful reproduction. Our results provide insight not only into the effects of captivity but can be broadly applicable for understanding the effects of environmental change on organisms and their gut microbiota, which we propose may require multiple generations to reach an alternative stable state.

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Sustained Drought, but Not Short-Term Warming, Alters the Gut Microbiomes of Wild Anolis Lizards

Abstract: As climate change progresses, it is crucial to understand how animals will respond to shifts in their local environments. One component of this response involves changes in the microbial communities living in and on host organisms.

Cited by 14 publications

References 91 publications

Warming effects on lizard gut microbiome depend on habitat connectivity

Warming effects on lizard gut microbiome depend on habitat connectivity

Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats

Environmental change drives multi-generational shifts in the gut microbiome that mirror changing animal fitness

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