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'Multisensory Ecology': Understanding adaptive trade-offs between vision and olfaction

Periodic Reporting for period 1 - MUSE ('Multisensory Ecology': Understanding adaptive trade-offs between vision and olfaction)

Reporting period: 2016-08-29 to 2018-08-28

Sensory systems enable animals to perceive their worlds and make adaptive decisions for survival. Evolution has shaped animals with multiple sensory systems that fit their lifestyle and environment, to give them the information they need to enhance their survival and reproduction. However, finding out about the world outside is energetically expensive: it involves complex sensory systems to collect the information, and dedicated neural systems to process it. Therefore, the benefits of acquiring information need to be balanced against the costs of receiving and processing it. As a consequence, when environmental constraints (e.g. living in the dark) limit the usefulness of specific sensory modalities (e.g. vision), shifts in investment in different sensory modalities can occur. For example, naked mole-rat are blind and compensate this lack of vision with an Eimer's organ that provides them with extra-sensory abilities in mechanosensory perception. Although comparative studies between closely related species have identified potential trade-offs between sensory modalities, empirical evidence is urgently needed to help establish that these trade-offs occur, and if so, under what conditions. Indeed, since human activity is shifting animals' lifestyle to a more nocturnal lifestyle, it becomes increasingly important to know how animals’ sensory capabilities will change to perceive the world around them.
Using brain measures, the project established the putative trade-off between vision and olfaction across a range of diurnal insect species, and identified that hunting mode and could help to explain how this trade-off is resolved. I found that predatory insects tend to invest more in vision and less in olfaction compared to insect species foraging by other methods. Using an empirical approach, I also found that living in the dark can reduce not just investment in vision, but also the reduce the size of the brain itself. This empirical approach also provided insights into how natural selection acts on sensory and neural systems, and showed the speed with which changes in the brain occur, and the degree to which these changes are reversible.
I collected the brains from a wide range of insect species, and confirmed a trade-off between the size of the visual and olfactory centres in the brain across a large range of insect species. I identified that foraging mode could be an important selection pressure acting on this trade-off, which is an important step in understanding why animals invest in different sensory systems (paper to be submitted to Current Biology, December 2018).
Using an empirical approach, I also made observations of this sensory trade-off by examining the brains of the Dark-flies. Using this novel and unique model system, I have demonstrated that individuals have been selected with a relative reduced investment for vision and an increased investment for olfaction. This paper has been submitted to Proc R Soc B (October 2018), and data were also presented at two international conferences (Ento ’17 International Symposium and National Science Meeting at Newcastle University, September 2017; International Congress of Neuroethology (ICN) 2018 in Brisbane (Australia), August 2018).
I also used the Dark-flies to test how quickly selection acts on sensory systems, whether the changes occured simultaneously in visual and olfactory systems, and if changes in investment in sensory systems could be reversible. I found that for Dark-flies put back in the light for 65 generations, investment was shifted towards the visual system becoming relatively more important to the detriment of olfaction (in prep. for Current Biology), confirming our preditions.
Additionally, I also established the genetic basis for the differences in size in areas of the brain that I had observed, and established how it was hereditary (article in preparation for Evolutionary Ecology); and if the differences in brain size between fly strains were related to energy consumption (article in preparation for a special issue in Brain, Behaviour and Evolution).
Our project fully addressed our main question and established a clear trade-off between vision and olfaction. By judiciously choosing to work with Dark-flies, I have not only shown a correlation in my comparative study across insect species, but have experimentally shown how selection acts on neural structures underpining sensory processing for the first time, using an empirical model system. The Dark-flies provides me with a unique model system for building my research niche in “multisensory ecology”, and opens up exciting new angles for research in how natural selection acts on the brain.
From our results, we may expect species adopting a nocturnal lifestyle to increase their olfactory capabilities to the detriment of their visual capabilities, and impacts on species becoming nocturnal may be more far-reaching than previously thought.
Trade-off between vision and olfaction over generation when light conditions change