Intrasexual competition modulates heatwave effects on male reproduction in Drosophila prolongata

Technical Summary: Intrasexual Competition Modulates Heatwave Effects on Male Reproduction in Drosophila prolongata

Problem Statement
Heatwaves are increasing in frequency and intensity, posing a severe threat to biodiversity by elevating mortality and impairing reproduction. While the direct physiological impacts of heat stress are well-documented, the extent to which these effects are modulated by environmental context remains poorly understood. Specifically, there is a gap in knowledge regarding the interaction between thermal stress and intraspecific competition. While competition can suppress individual condition and potentially reduce heat tolerance, it is unclear whether the intensity of male–male competition exacerbates or mitigates the negative reproductive consequences of extreme heat events. This study addresses this gap by investigating the combined effects of heatwaves and intrasexual competition on male reproductive output and survival in the territorial fruit fly, Drosophila prolongata.

Methodology
The researchers employed a fully factorial experimental design using D. prolongata, a species native to cool, montane habitats in Southeast Asia and known for aggressive male–male contests.

• Subjects: Wild-derived, outbred experimental males were reared under standard laboratory conditions (19°C) until sexual maturation.
• Treatments:
  • Thermal: Males were exposed to either a control temperature (19°C) or a simulated heatwave (28°C during the day, 19°C at night) for five consecutive days during sexual maturation.
  • Competition: Within each thermal treatment, males were housed in either "small groups" (3 males per vial, low competition) or "large groups" (10 males per vial, high competition).
• Assays:
  • Reproductive Output: Following the treatment period, each male was mated with a single unmated female. Researchers quantified total offspring (eggs and larvae), hatching success, and the proportion of larvae produced.
  • Survival: Post-mating, males were subjected to a starvation resistance assay (no food, agar media) to measure longevity.
  • Morphology: A subset of males was dissected to measure testis surface area as a proxy for sperm production investment.
• Analysis: Statistical models (GLMMs) accounted for temperature, group size, their interaction, and block effects. Overdispersion in count data was addressed using Conway–Maxwell–Poisson distributions.

Key Results

• Hatching Success: Exposure to the heatwave significantly reduced egg hatching success by 39.4% compared to controls. This effect was independent of group size.
• Larval Production (Reproductive Output): While the total number of offspring did not differ significantly across groups, the proportion of larvae produced showed a significant interaction between heat and competition.
  • In small groups (low competition), heatwave exposure caused a severe reduction in larval production.
  • In large groups (high competition), the negative impact of the heatwave on larval production was significantly attenuated. Males in large groups under heat stress produced more larvae than males in small groups under the same heat stress, though still fewer than control males.
• Survival: Contrary to the hypothesis that terminal investment would reduce survival, males exposed to the heatwave showed increased resistance to starvation (surviving ~6.26% longer) compared to controls. Group size and the interaction term had no significant effect on starvation resistance.
• Testis Size: Neither heat treatment, group size, nor their interaction affected testis size, suggesting that the observed changes in reproductive output were not mediated by gross differences in testis development during the maturation period.

Significance and Claims
The paper claims that the impact of extreme heat on reproduction is not solely a function of physiological thermal limits but is significantly shaped by social context. The primary finding is that intense intrasexual competition partially mitigates the negative effects of heat stress on male reproductive output.

The authors interpret this as a compensatory response where males facing stronger competition increase their reproductive investment (potentially via behavioral or physiological adjustments in sperm allocation or mating effort) specifically when subjected to the additional stress of a heatwave. This suggests that the "terminal investment" hypothesis (shifting resources to current reproduction at the cost of survival) may apply to reproductive output but was not reflected in the measured starvation resistance.

The study emphasizes that evaluating the risk of extreme climatic events to wildlife requires moving beyond single-stressor frameworks. The interaction between heat stress and competition intensity can alter population-level outcomes; for instance, populations at higher densities might appear less vulnerable to heatwaves than predicted by physiological models alone because individuals may upregulate reproductive investment under combined stressors. However, the authors note this mitigation is only partial, as heat-stressed males in competitive environments still produced fewer offspring than those in benign conditions.

Conclusion
The research highlights that biotic interactions, specifically intrasexual competition, can modulate the severity of abiotic stressors like heatwaves. The authors conclude that understanding how environmental context influences the response to extreme events is crucial for predicting the resilience of wildlife populations to climate change. They advocate for future research to explore similar interactive effects with other variables such as resource abundance, predation risk, and pathogen exposure.