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Stage- and Sex-Specific Impact of Heat Stress on – Reproductive Performance in Drosophila melanogaster

Meena, Abhishek. Stage- and Sex-Specific Impact of Heat Stress on – Reproductive Performance in Drosophila melanogaster. 2024, University of Zurich, Faculty of Science.

Abstract

Extreme temperature events are becoming more frequent and intense, posing significant threats to biodiversity, particularly on insects and other ectothermic species whose physiology and metabolism is dictated by ambient temperatures. Many studies have indicated that heat stress not only impacts the survival of organisms but also induces infertility or lower reproductive output at temperatures far below critical thermal limits. While most evidence surrounding the detrimental effects of heat stress comes from studies on either developmental or adult stages or within a single sex, much less known about how the timing of frequent heat events affects sex-specific reproductive stages, short or longer-term consequences, or how these effects interact between the sexes. This dissertation investigates the effect of heat stress on sex and stage-specific reproductive fitness, focusing on both short-term and long-term consequences as well as the underlying mechanisms, using Drosophila melanogaster as a model system. This work, combined in this thesis, is divided into the following three chapters.

Chapter 2 explores the cumulative effects of repeated heatwaves across life stages on male reproductive fitness. Previous studies have mostly examined the consequences of heat stress at either the juvenile or adult stages, and almost always focused on the immediately stress response. Our research addressed the short- and long-term consequences of repeated heat exposure across life stages; that is, including the patterns of post-stress recovery. Beyond measuring the fitness consequences and recovery dynamics, we also investigated several traits that could mediate heat-related fitness loss, such as sperm production and sperm viability, providing a mechanistic understanding of the observed effects. We found significant individual and combined effects of chronic juvenile and acute adult heat stress on male fitness traits. These effects were enhanced several days after the adult heat exposure, indicating only partial recovery or even delayed impacts. Further analyses revealed that reduced sperm production and impaired sperm function were the likely causes of these fitness declines. Overall, these findings suggest that repeated heat events can have lasting impacts on fertility, with important implications for short-lived organisms. Such effects have the potential to accelerate population declines in species sensitive to climate change.

Chapter 3 expands the previous chapters by investigating the impact of short-term heat stress at different developmental stages on the sex-specific reproductive performance of the adult flies. Most previous studies have used continuous heat stress within or between life stages, typically restricting their analysis to one sex or exploring both sexes collectively. These studies may not mimic the natural short-term heat stress and limits our understanding of stage and sex-specific reproductive consequences in short-lived organisms, as heat stress is rarely continuous over days or weeks. To address these knowledge gaps, we applied four hours of thermal treatment across a gradient of temperatures at seven distinct life stages, using shift-up-and-down approach, and then measured the sex-specific fitness consequences. Our results showed that males were more vulnerable than females, particularly during later stages of gamete development, which led to nearly complete reproductive failure at high sublethal temperatures. Even a brief heat exposure during sensitive stages resulted in a significant reduction in reproductive fitness. These findings underscore the importance of considering life stage- and sex-specific responses when assessing population persistence in climate change scenarios.

Chapter 4 investigates the impact of heat stress timing across distinct sex-specific reproductive stages (developmental, adult, and post-mating) on reproductive performance. While many studies have highlighted the vulnerability of gametes during development, pre-mating adult stages, or even within the female reproductive tract after mating, these studies often focus on individual stages or single sex or both sexes combined, leaving critical gaps in understanding how the timing of heat stress relative to sex-specific reproductive stages affects the reproductive performance of mating pairs. It remains unclear which reproductive stages are most sensitive to heat stress and how prior thermal history influences the sensitivity of gametes or their interactions between the sexes. To address these gaps, we exposed males and females to heat stress during development, as adults before mating, and females while storing sperm after mating. We then measured the reproductive performance of pairs in a full-factorial design between these different thermal treatments and their corresponding controls. Our results show that the thermal sensitivity of gametes increases as reproductive stages progress, leading to a 50% decline in reproductive performance after post-mating heat stress, regardless of prior thermal history of gametes. Additionally, cumulative heat exposure during both developmental and pre-mating adult stages caused a more pronounced decline in reproductive performance than heat exposure at individual stages. Among life stages, the pre-mating adult stage was more affected by heat exposure than developmental stages. Both sexes experienced negative impacts of heat stress, but females were more severely affected than males. These findings highlight the importance of considering the timing of heat stress in relation to reproductive stages when evaluating the effects of heat events on biodiversity, and they underscore the vulnerability of both sexes, particularly during post-mating stages.

In summary, this dissertation explores the fitness consequences of frequent heat stress events across distinct life stages in a sex-specific manner, showing the effects of cumulative heat stress across life stages on male reproductive fitness (chapter 2) and heightened thermal sensitivity of late juvenile stages, particularly in males (chapter 3). However, gametes are not only vulnerable before mating but also, and even more so, after mating, emphasizing the importance of the timing of heat stress on sex-specific reproductive stages (chapter 4).

Across my three data chapters, I demonstrate that the reproductive consequences of heat stress depend on the life stages and sex being exposed, enhanced by repeated heat exposure. This dissertation contributes new but important nuance to the field of thermal biology. By considering the timing of extreme temperature events relative to developmental and reproductive processes, sex differences in thermal sensitivity, recovery rates and the complex interactions between these factors, we are likely to achieve higher accuracy in predictions of population fitness and dynamics in the context of climate change. Throughout my dissertation I highlight and fill important knowledge gaps in the current literature and outline fruitful avenues and directions for future research to better understand the consequences of heat stress, and by extension climate change. While studying these processes in a model organism under strict lab conditions as a proof of concept, the questions addressed in my work may be even more significant for species whose populations are highly vulnerable to extreme heat events.

Additional indexing

Item Type:Dissertation (cumulative)
Referees:Lüpold Stefan, Blanckenhorn Wolf, Flatt Thomas
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
UZH Dissertations
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Place of Publication:Zürich
Date:27 December 2024
Deposited On:27 Dec 2024 10:58
Last Modified:27 Dec 2024 10:58
Number of Pages:198
OA Status:Green
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