Evolutionaire ecologie van geografische patronen in stresstolerantie bij een waterjuffer en haar darmmicrobioom

Biodiversity is under increasing pressure from multiple stressors, such as warming, pesticide pollution, and pathogen exposure. The ability of organisms to cope with such challenges depends not only on their own phenotype, or their own life history, behavioural, and physiological traits that collectively form their pace-of-life, but also on their gut microbiome. In particular, the gut microbiome has shown to profoundly influence host fitness, shaping key host traits, and furthermore has been put forward as a potential contributor to the host's stressor tolerance. Freshwater ecosystems are among the most threatened habitats on Earth, wherein damselflies are ideal model organisms with their complex aquatic-terrestrial life cycle, ecological importance, and natural variation in pace-of-life across environmental gradients. Consequently, they bridge ecosystems and face stressors, even across life stages. Their microbiome gets shaped by multiple environments across their entire life, potentially impacting their life history and stressor tolerance, even across ecosystems. Through a combination of common garden and field experiments, whereby life history, behavioural and physiological measurements were performed, together with microbiome sequencing and gut microbiome transplants, using two congeneric species, Ischnura elegans and I. pumilio, this work shows that the gut microbiome plays a fundamental role for its host. This thesis shows partial evidence of a gut microbial influence on the pace-of-life of damselflies, and clear causal evidence of gut microbiota playing a fundamental role in shaping their stressor tolerance to warming, pesticide exposure, and pathogen infection. In more detail, across latitudinal and hydroperiod gradients, clear pace-of-life differentiation emerged: low-latitude I. elegans generally had a faster pace-of-life than high-latitude ones, while I. pumilio consistently had a faster pace-of-life than I. elegans. Extreme environmental conditions could mask these intrinsic differences, indicating that pace-of-life is generally fixed but can be altered by strong environmental influences. Warming had both positive and negative effects depending on population- and species-specific thermal adaptation. Extreme heat events and daily temperature fluctuations often pushed traits beyond optimal ranges, especially in mid- and high-latitude populations. Pesticide exposure consistently reduced performance, but effects varied in severity and species-specificity depending on physiological capacity, whereby, contrary to expectations, no synergistic effects of warming and pesticide exposure were observed, likely due to sequential exposure allowing recovery. Pathogen exposure reduced survival, and warming further increased mortality in thermally sensitive populations, showing that heat can magnify disease impacts without affecting pathogen growth. These results highlight that multiple stressor effects cannot be predicted from single-stressor studies alone and are shaped by multiple factors, such as local adaptation, exposure history, and physiological energy-based trade-offs. Furthermore, the gut microbiome showed high variability but consistent species- and latitude-specific patterns, even under common garden conditions, suggesting genetic influences and possible vertical transmission. Life stage strongly shaped microbiome diversity and composition, with filtering from bacterioplankton to larvae and partial retention into the adult stage. Stressor exposure altered microbiome diversity and composition in complex ways, sometimes increasing diversity through presence of new taxa, other times reducing it via loss of key bacteria. Changes in microbial communities often paralleled adaptive or maladaptive host responses, and microbiome transplants provided direct evidence for its causal role in their host's stressor sensitivity. Overall, this work underscores the intricate host-microbiome-environment interplay and the need for causal gut microbiome transplant experiments to understand microbiome-mediated stressor tolerance in a changing world. Moreover, this research underscores that predicting how species will respond to global change requires integrating host-microbiome interactions into eco-evolutionary studies. The gut microbiome emerges as both a mediator of stressor effects and a potential avenue for rapid adaptation, with implications for biodiversity conservation in an increasingly altered world.

Publication Details

Journal
Lirias (KU Leuven)
Published
2025-10-29
Primary Topic
Freshwater macroinvertebrate diversity and ecology
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article

Evolutionaire ecologie van geografische patronen in stresstolerantie bij een waterjuffer en haar darmmicrobioom

Lirias (KU Leuven)
Freshwater macroinvertebrate diversity and ecology
article

Evolutionaire ecologie van geografische patronen in stresstolerantie bij een waterjuffer en haar darmmicrobioom

article en

Abstract

Biodiversity is under increasing pressure from multiple stressors, such as warming, pesticide pollution, and pathogen exposure. The ability of organisms to cope with such challenges depends not only on their own phenotype, or their own life history, behavioural, and physiological traits that collectively form their pace-of-life, but also on their gut microbiome. In particular, the gut microbiome has shown to profoundly influence host fitness, shaping key host traits, and furthermore has been put forward as a potential contributor to the host's stressor tolerance. Freshwater ecosystems are among the most threatened habitats on Earth, wherein damselflies are ideal model organisms with their complex aquatic-terrestrial life cycle, ecological importance, and natural variation in pace-of-life across environmental gradients. Consequently, they bridge ecosystems and face stressors, even across life stages. Their microbiome gets shaped by multiple environments across their entire life, potentially impacting their life history and stressor tolerance, even across ecosystems. Through a combination of common garden and field experiments, whereby life history, behavioural and physiological measurements were performed, together with microbiome sequencing and gut microbiome transplants, using two congeneric species, Ischnura elegans and I. pumilio, this work shows that the gut microbiome plays a fundamental role for its host. This thesis shows partial evidence of a gut microbial influence on the pace-of-life of damselflies, and clear causal evidence of gut microbiota playing a fundamental role in shaping their stressor tolerance to warming, pesticide exposure, and pathogen infection. In more detail, across latitudinal and hydroperiod gradients, clear pace-of-life differentiation emerged: low-latitude I. elegans generally had a faster pace-of-life than high-latitude ones, while I. pumilio consistently had a faster pace-of-life than I. elegans. Extreme environmental conditions could mask these intrinsic differences, indicating that pace-of-life is generally fixed but can be altered by strong environmental influences. Warming had both positive and negative effects depending on population- and species-specific thermal adaptation. Extreme heat events and daily temperature fluctuations often pushed traits beyond optimal ranges, especially in mid- and high-latitude populations. Pesticide exposure consistently reduced performance, but effects varied in severity and species-specificity depending on physiological capacity, whereby, contrary to expectations, no synergistic effects of warming and pesticide exposure were observed, likely due to sequential exposure allowing recovery. Pathogen exposure reduced survival, and warming further increased mortality in thermally sensitive populations, showing that heat can magnify disease impacts without affecting pathogen growth. These results highlight that multiple stressor effects cannot be predicted from single-stressor studies alone and are shaped by multiple factors, such as local adaptation, exposure history, and physiological energy-based trade-offs. Furthermore, the gut microbiome showed high variability but consistent species- and latitude-specific patterns, even under common garden conditions, suggesting genetic influences and possible vertical transmission. Life stage strongly shaped microbiome diversity and composition, with filtering from bacterioplankton to larvae and partial retention into the adult stage. Stressor exposure altered microbiome diversity and composition in complex ways, sometimes increasing diversity through presence of new taxa, other times reducing it via loss of key bacteria. Changes in microbial communities often paralleled adaptive or maladaptive host responses, and microbiome transplants provided direct evidence for its causal role in their host's stressor sensitivity. Overall, this work underscores the intricate host-microbiome-environment interplay and the need for causal gut microbiome transplant experiments to understand microbiome-mediated stressor tolerance in a changing world. Moreover, this research underscores that predicting how species will respond to global change requires integrating host-microbiome interactions into eco-evolutionary studies. The gut microbiome emerges as both a mediator of stressor effects and a potential avenue for rapid adaptation, with implications for biodiversity conservation in an increasingly altered world.

Lirias (KU Leuven)
Life in Land
Openalex Percentile: Top 33%
Freshwater macroinvertebrate diversity and ecology
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