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      Eye size and investment in frogs and toads correlate with adult habitat, activity pattern and breeding ecology

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          Abstract

          Frogs and toads (Amphibia: Anura) display diverse ecologies and behaviours, which are often correlated with visual capacity in other vertebrates. Additionally, anurans exhibit a broad range of relative eye sizes, which have not previously been linked to ecological factors in this group. We measured relative investment in eye size and corneal size for 220 species of anurans representing all 55 currently recognized families and tested whether they were correlated with six natural history traits hypothesized to be associated with the evolution of eye size. Anuran eye size was significantly correlated with habitat, with notable decreases in eye investment among fossorial, subfossorial and aquatic species. Relative eye size was also associated with mating habitat and activity pattern. Compared to other vertebrates, anurans have relatively large eyes for their body size, indicating that vision is probably of high importance. Our study reveals the role that ecology and behaviour may have played in the evolution of anuran visual systems and highlights the usefulness of museum specimens, and importance of broad taxonomic sampling, for interpreting macroecological patterns.

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          Most cited references 63

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          The Ecology and Behavior of Amphibians

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            Energy limitation as a selective pressure on the evolution of sensory systems.

            Evolution of animal morphology, physiology and behaviour is shaped by the selective pressures to which they are subject. Some selective pressures act to increase the benefits accrued whilst others act to reduce the costs incurred, affecting the cost/benefit ratio. Selective pressures therefore produce a trade-off between costs and benefits that ultimately influences the fitness of the whole organism. The nervous system has a unique position as the interface between morphology, physiology and behaviour; the final output of the nervous system is the behaviour of the animal, which is a product of both its morphology and physiology. The nervous system is under selective pressure to generate adaptive behaviour, but at the same time is subject to costs related to the amount of energy that it consumes. Characterising this trade-off between costs and benefits is essential to understanding the evolution of nervous systems, including our own. Within the nervous system, sensory systems are the most amenable to analysing costs and benefits, not only because their function can be more readily defined than that of many central brain regions and their benefits quantified in terms of their performance, but also because recent studies of sensory systems have begun to directly assess their energetic costs. Our review focuses on the visual system in particular, although the principles we discuss are equally applicable throughout the nervous system. Examples are taken from a wide range of sensory modalities in both vertebrates and invertebrates. We aim to place the studies we review into an evolutionary framework. We combine experimentally determined measures of energy consumption from whole retinas of rabbits and flies with intracellular measurements of energy consumption from single fly photoreceptors and recently constructed energy budgets for neural processing in rats to assess the contributions of various components to neuronal energy consumption. Taken together, these studies emphasize the high costs of maintaining neurons at rest and whilst signalling. A substantial proportion of neuronal energy consumption is related to the movements of ions across the neuronal cell membrane through ion channels, though other processes such as vesicle loading and transmitter recycling also consume energy. Many of the energetic costs within neurons are linked to 3Na(+)/2K(+) ATPase activity, which consumes energy to pump Na(+) and K(+) ions across the cell membrane and is essential for the maintenance of the resting potential and its restoration following signalling. Furthermore, recent studies in fly photoreceptors show that energetic costs can be related, via basic biophysical relationships, to their function. These findings emphasize that neurons are subject to a law of diminishing returns that severely penalizes excess functional capacity with increased energetic costs. The high energetic costs associated with neural tissue favour energy efficient coding and wiring schemes, which have been found in numerous sensory systems. We discuss the role of these efficient schemes in reducing the costs of information processing. Assessing evidence from a wide range of vertebrate and invertebrate examples, we show that reducing energy expenditure can account for many of the morphological features of sensory systems and has played a key role in their evolution.
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              Visual Ecology

              Visual ecology is the study of how animals use visual systems to meet their ecological needs, how these systems have evolved, and how they are specialized for particular visual tasks. This book provides the first up-to-date synthesis of the field to appear in more than three decades. Featuring some 225 illustrations, including more than 140 in color, spread throughout the text, the book begins by discussing the basic properties of light and the optical environment. It then looks at how photoreceptors intercept light and convert it to usable biological signals, how the pigments and cells of vision vary among animals, and how the properties of these components affect a given receptor's sensitivity to light. The book goes on to examine how eyes and photoreceptors become specialized for an array of visual tasks, such as navigation, evading prey, mate choice, and communication. A timely and much-needed resource for students and researchers alike, the book also includes a glossary and a wealth of examples drawn from the full diversity of visual systems.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc Biol Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                30 September 2020
                23 September 2020
                23 September 2020
                : 287
                : 1935
                Affiliations
                [1 ]Department of Life Sciences, The Natural History Museum , London SW7 5BD, UK
                [2 ]Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution , Washington, DC 20560-0162, USA
                [3 ]Department of Herpetology, California Academy of Sciences , San Francisco, CA 94118, USA
                [4 ]Department of Biology, Amphibian and Reptile Diversity Research Center, The University of Texas at Arlington , Arlington, TX 76019, USA
                Author notes

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5113670.

                Article
                rspb20201393
                10.1098/rspb.2020.1393
                7542830
                32962540
                © 2020 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                Product
                Funding
                Funded by: Natural Environment Research Council, http://dx.doi.org/10.13039/501100000270;
                Award ID: NE/R002150/1
                Funded by: Division of Environmental Biology, http://dx.doi.org/10.13039/100000155;
                Award ID: DEB-#1655751
                Categories
                1001
                70
                60
                Evolution
                Research Article
                Custom metadata
                September 30, 2020

                Life sciences

                allometry, anurans, amphibians, morphological evolution, sensory evolution, visual ecology

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