Temperature fluctuations during development reduce male fitness and may limit adaptive potential in tropical rainforest Drosophila

Abstract

Understanding the potential for organisms to tolerate thermal stress through physiological or evolutionary responses is crucial given rapid climate change. Although climate models predict increases in both temperature mean and variance, such tolerances are typically assessed under constant conditions. We tested the effects of temperature variability during development on male fitness in the rainforest fly Drosophila birchii, by simulating thermal variation typical of the warm and cool margins of its elevational distribution, and estimated heritabilities and genetic correlations of fitness traits. Reproductive success was reduced for males reared in warm (mean 24 °C) fluctuating (±3 °C) vs. constant conditions but not in cool fluctuating conditions (mean 17 °C), although fluctuations reduced body size at both temperatures. Male reproductive success under warm fluctuating conditions was similar to that at constant 27 °C, indicating that briefly exceeding critical thermal limits has similar fitness costs to continuously stressful conditions. There was substantial heritable variation in all traits. However, reproductive success traits showed no genetic correlation between treatments reflecting temperature variation at elevational extremes, which may constrain evolutionary responses at these ecological margins. Our data suggest that even small increases in temperature variability will threaten tropical ectotherms living close to their upper thermal limits, both through direct effects on fitness and by limiting their adaptive potential.

Terrestrial insects and climate change: adaptive responses in key traits

“…In the neotropical pseudoscorpion, males produced 45% less sperm at temperatures mimicking 3.5 ∘ C of warming (Zeh et al, 2012). The temperature sensitivity of male sperm and the extent to which species can shift male sterility remains a poorly understood phenomenon (David et al, 2005;Zeh et al, 2012;Saxon et al, 2018). Thermal sensitivities may also differ across life stages (Sinclair et al, 2016;Zhao et al, 2017) and Kingsolver et al (2011) have shown that larvae and pupae of Manduca sexta have different thermal sensitivities and differ in their TPC.…”

Hawaiian picture‐winged Drosophila exhibit adaptive population divergence along a narrow climatic gradient on Hawaii Island

“…Twelve picture-winged Drosophila species are currently listed as endangered or threatened, and monitoring over the last 30 years has documented sharp declines and reduced distributions for many of the nonlisted species (Richardson, 2006). These Drosophila, like many tropical ectotherms, are thought to be particularly vulnerable to climatic changes due to their narrow physiological tolerance windows (Saxon, O'Brien, & Bridle, 2018), as well as limited habitat ranges and highly specific native host plant associations (Magnacca, Foote, & O'Grady, 2008;Magnacca & Price, 2015).…”

Transgenerational and within‐generation plasticity shape thermal performance curves

“…Mean global temperatures, thermal variability, and the frequency of extreme environmental events have increased, and these have had significant impacts on biodiversity (Dawson, Jackson, House, Prentice, & Mace, ; Gitay, Suárez, Watson, & Dokken, ; Meehl & Tebaldi, ; Pachauri & Reisinger, ; Palmer et al, ; Vázquez, Gianoli, Morris, & Bozinovic, ). These changes in the thermal environment are expected to be particularly challenging for ectotherms because their physiology is directly dependent on ambient temperatures (Pörtner, ; Saxon, O'Brien, & Bridle, ; Sunday, Bates, & Dulvy, ). To a large extent the susceptibility and vulnerability of ectotherms to climate change has been assessed through the study of thermal performance curves (TPCs) which characterize the relationship between performance or fitness and body temperature (Sinclair et al, ).…”

“…These changes in the thermal environment are expected to be particularly challenging for ectotherms because their physiology is directly dependent on ambient temperatures (Pörtner, 2002;Saxon, O'Brien, & Bridle, 2018;Sunday, Bates, & Dulvy, 2011). To a large extent the susceptibility and vulnerability of ectotherms to climate change has been assessed through the study of thermal performance curves (TPCs) which characterize the relationship between performance or fitness and body temperature (Sinclair et al, 2016).…”

“…When environmental conditions change over short time scales, individuals can exhibit continuous and reversible phenotypic transformations (Piersma & Drent, 2003). During the early ontogeny, organisms are highly sensitive to environmental cues (Burggren & Mueller, 2015;Saxon et al, 2018;Spicer, Rundle, & Tills, 2011). Thus, developmental conditions can induce modifications in phenotype and potentially lead to irreversible changes (Burggren, 2018;Cooper, Tharp, Jernberg, & Angilletta, 2012;Dufty, Clobert, & Møller, 2002).…”