Thesis Project: The exploration of thermal landscapes in Drosophila adapted to different thermal regimes

I. Introduction and background

Current theory regarding thermal adaptation of ectothermic animals poses few generalizations that can apply to all lineages. One is that virtually all physiological functions studied to date, and based on the speed or power of muscle contraction (but not force),  can be represented as an asymmetrical function relating performance to temperature. These curves exhibit various degrees of flexibility to shifts in average temperature in the contexts of adjustment (acclimation), adaptation (Angilletta, Niewiarowski et al. 2002; Navas 2004) or experimental selection (Huey and Kingsolver 1993). More recently, thermal variance gained importance as a relevant concept in ecology, for example contextualizing Janzen’s influential paper on mountain passes (Janzen 1967) into current views on evolutionary thermal biology (Ghalambor, Huey et al. 2006).  Empirical data promoted further interest in thermal variance by showing that elevational gradients in tropical areas involve dramatic changes not only in the body temperature of ectothermic animals, but also on the variance of activity temperature and daily cycles of body temperature (Navas, Carvajalino-Fernández et al. 2013). A pattern towards increased thermal variance at high-elevation is typical of tropical systems but, convergences at microhabitat scale exist with alpine systems (Diemer 1996), which are also affected by strong seasonal variation.

Studies on thermal variation have addressed questions related mainly to evolution of life history (Shine 2004) and performance curves (Kingsolver, Izem et al. 2004), and more recently, to the adaptive value of phenotypic plasticity as a response to thermal variation varying in predictability (Manenti, Sorensen et al. 2014). For example high-elevation tropical anurans display evolutionary convergence across and within genera as suggested by the common denominator of flat, eurythermic performance curves relative to low-elevation counterparts (Navas, Gomes et al. 2008). In contrast, findings with Drosophila show patterns of adaptation among species exposed to both fixed and fluctuating thermal regimes (Loeschcke, Bundgaard et al. 1999). Studies with Drosophila have enhanced discussion on the evolution of thermal biology in fluctuating environments, and pointed out important limits to our understanding of the problem. One most intriguing finding is that artificial fluctuating environments fail to reproduce the adaptive patterns they aim to mimic, for example in the context of clinal natural variation in D. melanogaster (Kellermann, Hoffmann et al. 2015). Therefore, despite the extreme value of artificial selection and studies along clines, questions remain regarding adaptation to thermally fluctuating environments.

Among terrestrial environments, a most important cline enhancing thermal variability is altitude. A typical tropical altitudinal gradient, for example, involves enhanced temporal and special heterogeneity in temperature (Navas, Carvajalino-Fernández et al. 2013). The fact that variation involves both time and space is germane for discussion. Artificial selection and experiments in general, have traditionally focused on the temporal component of thermal heterogeneity. That temporal and special variation are integrated into one behavioural-physiological component is a long-standing idea in the literature (Hutchison and Manes 1979), yet it has been neglected. Experiments exposing animals to temporally fluctuating environments isolate responses to temporal variation, but say nothing about the ability of animals to navigate complex thermal landscapes (e.g., Cunnington, Schaefer et al. 2008), a factor that seems important when analyzing thermal adaptation (Sears, Raskin et al. 2011). It is possible, therefore, that artificial and natural selection are not expected to convey similar results for the latter involve exposure to both temporal and spatial gradients, and therefore, a behavioral component. The finding that acclimation to fluctuating environments is linked to both physiological and behavioral responses, opens promising, interesting and needed research.

II.                         Objectives

We propose a study with Drosophila in which we test hypotheses regarding behavioral and physiological traits in species artificially adapted to thermally fluctuating environments (time only) and to naturally variable environments (time and space). Our hypotheses are:

a) Drosophila artificially evolved under thermal variance mimicking natural variance display lower tendency to explore thermal landscapes than naturally adapted counterparts do, but similar to flies reared under constant temperature. In other words, experimental evolution does not influence the tendency to explore thermal behavior, but natural selection does.

b) Even in the context of the above premise, all groups tend to explore more thoroughly sub-optimal cold temperatures (not near lethal) than sub-optimal warm temperatures (near lethal).

c) If finding sites for reproduction of equal quality involves circulating through suboptimal temperatures, sites would be preferred that require circulation through colder suboptimal temperatures than to warmer suboptimal temperatures. However, overall reproductive output after crossing thermal barriers will be higher in flies evolved under natural selection.

d) The drive to explore thermal environments is an inheritable trait.

Details of Methods (behavioral tests and artificial selection studies) have been worked out under a recent visit of Carlos Navas in Aarhus. The species chosen will be Drosophila melanogaster kept at either constant 23 C or at fluctuating temperatures with a mean of 23 C.

Co-supervisor: CARLOS A. NAVAS: Professor at the Department of Physiology of Biosciences Institute, University of São Paulo (IB-USP), Brazil. He is a physiological ecologist who has worked mainly on the impact of climate change on the fauna, with emphasis on amphibians, reptiles and arthropods.

Carlos A. Navas is internationally well known for his contributions to thermal biology and its physiological foundations (see https://scholar.google.com.br/citations?user=TYtNw3cAAAAJ&hl=pt-BR).

Contact: Volker Loeschcke and Carlos Navas (Sao Paulo, Brazil)

The project proposal has been submitted 28.10.2020.