Mike Cullen award: animal responses to stressor interactions

As this year’s winner of the Mike Cullen Research Fellow Award, Lesley Alton was awarded $5000 in research funds for her publication with Vanessa Kellerman that appeared in Nature Climate Change in 2023.

Professor Mike Cullen was Chair of Zoology at Monash from 1976 to 1992. He was a passionate advocate for early career researchers and also instrumental in bringing a more rigorous and quantitative approach to the behavioural sciences. The awards committee felt that Lesley and Vanessa’s publication was strongly aligned with Mike Cullen’s values.

But of course, science doesn’t just happen overnight and, in the Mike Cullen Lecture, Lesley detailed the trajectory of her research interests and how they led her to this point.

Lesley started her PhD at the University of Queensland in 2007 just after the first global assessment of amphibians had taken place. The assessment confirmed a global decline in amphibians including from seemingly pristine habitats. One of the competing hypotheses for amphibian declines was increased exposure to UV-B radiation associated with human-induced stratospheric ozone depletion. Lesley already knew that UV-B could have adverse effects on amphibian development when she started her PhD, but in nature, animals face many challenges, and so Lesley wanted to know if other sources of environmental stress interact with UV-B to have compounding negative effects on amphibians.

Lesley was not surprised to find that UV-B decreased survival in tadpoles but she was surprised to find that exposure to UV-B in combination with predatory cues decreased tadpole survival even further. She wondered if simultaneous exposure to these two stressors carried a greater metabolic cost than exposure to either of these stressors in isolation. By studying both the metabolic and behavioural responses of tadpoles to these stressors, Lesley found evidence that being exposed to UV-B is more energetically costly for tadpoles when they live with predators: tadpoles exposed to both stressors were less active, yet their metabolic rates remained elevated suggesting they were under more physiological stress than those exposed only to UV-B.

Lesley’s interests in the effects of UV-B continued when she took up her first postdoctoral position at Monash University, but this time she was interested in how it might affect mosquitoes. With UV-B predicted to increase in the tropics by the end of the century, Lesley wondered how this might affect the ability of mosquitoes to transmit pathogens like dengue virus, which is a growing threat to human populations living in tropical and subtropical regions. To study the effects of UV-B on mosquitoes, Lesley exposed developing mosquito larvae to very low doses of UV-B every day to determine if early-life exposure to UV-B could have long lasting effects on adult immune function and fitness. Worryingly, Lesley found that a UV-B dose that is 10­–30 lower than what is currently observed in the tropics made female mosquitoes much more likely to become infected with dengue virus, but it also reduced their survival and fecundity – an unexpected bonus for tropical regions?

Lesley found that exposure to UVBR during a mosquitos development resulted in slower development, higher dengue infection but lower fecundity and higher mortality.

In addition to her work on UV-B, Lesley also developed an interest in the effect of temperature on the metabolic rates of cold-blooded animals (ectotherms), which rely on the thermal conditions of their environment to regulate their body temperature. This interest began while working as a research assistant at the University of Queensland when she received a Journal of Experimental Biology Travelling Award to visit a lab group in the USA. This group were looking at the effects of temperature on the evolution of traits in fruit flies. So, another change of model species, but the trip allowed Lesley to use her expertise in measuring metabolic rates to test the century-old Metabolic Cold Adaptation Hypothesis. This hypothesis predicts that animals evolved at cold temperatures will have higher metabolic rates than those evolved at hot temperatures when measured together at the same temperature. This counter-intuitive effect of temperature on the evolution of metabolic rate is predicted to arise as a consequence of natural selection counteracting the slowing down of metabolic rate that occurs at colder temperatures by favouring those individuals with higher metabolic rates. However, because patterns consistent with the Metabolic Cold Adaptation Hypothesis are not always evident in nature, the hypothesis remains highly controversial.

By measuring the metabolic rates of flies that had evolved experimentally in the lab at different temperatures, Lesley conducted a robust test of the Metabolic Cold Adaptation Hypothesis, but did not find support for the hypothesis. Lesley is now investigating whether the Metabolic Cold Adaptation Hypothesis is borne out if flies evolve at different temperatures under conditions where food is more limited, a scenario that more accurately reflects nature.

We will have to wait and see whether temperature and nutrition interact to shape the evolution of metabolic rate in fruit flies. Lesley has also examined whether environmental factors influence the capacity of ectotherms to respond to climate warming through acclimation which, unlike evolution, occurs within an animal’s lifetime. While ectotherms are expected to have higher energy demands in a warmer world, many ectotherms can acclimate to higher temperatures by reducing the thermal sensitivity of their metabolic rates to offset these energy requirements to some extent. However, Lesley and Vanessa’s research in fruit flies has shown that nutritionally poor diets and species interactions can erode the energetic benefits of thermal acclimation.

Lesley and Vanessa reared the larvae of three Drosophila species in single-species or two-species cultures with limited food to promote competition.

A more in-depth summary of the award-winning publication on the effect of species interactions on the metabolic costs of climate warming demonstrates that to improve our understanding of the threat of climate warming to species we must study animal responses to temperature in combination with other environmental stressors.

After adult flies emerged from our cultures, the team measured the metabolic rate and activity of nearly 400 adult female flies using a multi-channel flow-through respirometry system and Drosophila activity monitors.

This research is published in the journal Nature Climate Change.