Lessons Learned From Comparative and Evolutionary Physiology Hannah V. Carey
Physiology 30:80-81, 2015. doi:10.1152/physiol.00003.2015 You might find this additional info useful... This article cites 10 articles, 10 of which can be accessed free at: /content/30/2/80.full.html#ref-list-1 Updated information and services including high resolution figures, can be found at: /content/30/2/80.full.html Additional material and information about Physiology can be found at: http://www.the-aps.org/publications/physiol
This information is current as of March 18, 2015.
Downloaded from on March 18, 2015
Physiology (formerly published as News in Physiological Science) publishes brief review articles on major physiological developments. It is published bimonthly in January, March, May, July, September, and November by the American Physiological Society, 9650 Rockville Pike, Bethesda, MD 20814-3991. Copyright © 2015 by the American Physiological Society. ISSN: 1548-9213, ESSN: 1548-9221. Visit our website at http://www.the-aps.org/.
PHYSIOLOGY’S IMPACT
Hannah V. Carey University of Wisconsin-Madison, Madison, Wisconsin
PHYSIOLOGY 30: 80 – 81, 2015; doi:10.1152/physiol.00003.2015
Lessons Learned From Comparative and Evolutionary Physiology
80
echolocating bats and toothed whales, a stunning example of how evolution produced a remarkable level of similarity in the sensing of prey with ultrasound in two disparate animal groups Despite their extreme differences in size (very large, very small) and environment (water and air), bats and toothed whales use similar call frequencies and acoustic behavior while foraging in dark environments. In a similar vein, Price and colleagues (9) explain how the relatively smaller intestines of flying birds and bats, a trait likely driven by the selective pressure to reduce body mass to overcome gravity, constrains the capacity for digestion and absorption. Recent studies suggest both birds and bats compensate by having higher amplification of their intestinal villi and by having relatively high rates of paracellular as opposed to transcellular, transporter-mediated nutrient absorption. The selective pressures of aerial lifestyles were apparently solved in quite similar ways in these two vertebrate classes. Diversity in mechanisms of oxygen uptake and distribution in two animal phyla are described by Panneton (8) and Harrison et al. (4). The comparative approach has led to in-depth understanding of the mechanics of the diving response, a reflex that is found in all vertebrates but is most well developed in aquatic species (8). This combination of three independent reflexes that enhance survival in low-oxygen conditions involves redistribution of blood flow through peripheral vasoconstriction, such that oxygenated blood is directed preferentially to the central nervous system and heart at the expense of cutaneous, muscular, and splanchnic circulations. Oxygen uptake in insects is ancient and elaborate, and differs substantially from mammalian systems, with greater capacity for oxygen delivery from air to cells by either diffusive or convective mechanisms, and marked differences in morphological and structural components (4). Knowledge of these highly successful insect fluidic sys-
1548-9213/15 ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc.
Downloaded from on March 18, 2015
Comparative physiology is the exploration of physiological principles through examination of the functional diversity among animal species. Because diversity derives from evolution and natural selection, the work comparative physiologists do often extends beyond characterizing a physiological system at the mechanistic level to consideration of how the mechanism is relevant in an ecological or evolutionary context. One of the major goals of the field is to determine what ecological pressures have led to a particular physiological adaptation having a selective advantage, and how selective pressures have produced the differences (and similarities) we see among different species. For the most part, comparative physiologists choose study animals that diverge from the conventional laboratory species, with the gold standard being the ability to study physiology in free-living animals behaving in their natural environments. Thus the physiology underlying comparative studies tends to be more closely associated with responses to reallife challenges that are often not possible to replicate in the caged setting or in animals that have been bred for many generations to thrive in a caged environment where they are exposed to generic ambient housing conditions. Sometimes comparative physiology questions take this literally to the extreme by using species that live in highly challenging environments (e.g., deserts, high elevation, polar regions, deep oceans). Several recent articles published in Physiology highlight how comparative physiologists are identifying physiological solutions to ecological problems that have evolved in diverse groups of animals. They provide us with lessons to be learned on several fronts. Comparative approaches are particularly powerful when they reveal how fundamental ecological challenges have led to convergence in physiological pathways. Madsen and Surlykke (6) describe the convergence in biosonar systems in
tems can serve as bioinspiration for such fields a microfluidics, nanofabrication, and tissue engineering (4). Using comparative physiology to elucidate nature’s solutions to biomedical problems has a long history and is the foundation of the Krogh Principle (1). Although sometimes mentioned as a constraint for experimentation, the diverse genetic background of most species used in comparative physiology research makes these species very appropriate as animal models for human biomedical investigation. The heterogeneous natures of human populations in terms of genetics, epigenetic landscape, and the range of environmental factors that can affect physiology and health are more in tune to species that are living or are recently derived from wild populations, as opposed to conventional, laboratory-bred animals. Furthermore, the mechanisms by which certain animals thrive in environments we humans consider “extreme” can provide new avenues to pursue in the management of recalcitrant medical challenges. Many of the comparative reviews published in Physiology illustrate these principles very well. Understanding how and why skeletal systems evolved in diverse groups of vertebrates may provide new approaches for treatments of skeletal diseases, such as osteoporosis (2). The evolutionary and ecological bases for persistence or lack of circadian cycles in polar species may contribute to better treatment for circadian disorders in humans (10). Unraveling the complexity of osmoregulatory systems in fish may provide clues to treat fluid and electrolyte disorders (5). Identifying mechanisms that control the diving response can shed light on how the mammalian brain controls autonomic function and contributes to preservation of tissue oxygenation in nondiving species (8). Comparative physiology can also contribute to biomedical research by aiding the appropriate design of housing facilities for conventional laboratory animals. Maloney and colleagues (7) point out that inadequate understanding of an animal’s thermal biology can result in housing temperatures that, although comfortable for humans, are outside of the thermal neutral zone for the particular species. For example, the increased met-
imals, used in parallel with collars that monitor amount and type of light exposure, are helping to resolve why circadian rhythmicity in some polar vertebrates persists under conditions of continuous light or dark, but not in others (10). The importance of studying animal physiology in the field and the technology that supports field physiology are major themes of the review by Fuller et. al., who address adaptations to heat and water storage in large, arid-zone mammals (3). The ability to monitor both environmental and body temperatures in the wild where animals can select the microclimates they prefer has led to a new appreciation for “selective brain cooling” (SBC), which was long thought to be an important mechanism to protect the brain from hyperthermic damage in hot environments. In fact, biologging studies have shown that animals may abandon SBC during high-intensity exercise when brain temperatures climb as high as 42°C, perhaps to balance thermoregulatory and osmoregulatory needs. Research like this on free-ranging animals is needed to inform management decisions for species particularly vulnerable to changing environments, be they due to climate change, habitat destruction, or other anthropomorphic alterations to the planet. Beyond the generation of new knowledge and its potential application to fields like bioengineering and biomedicine, comparative physiology is enormously valuable in generating interest in animal biology in general, and physiology in particular, to students and the lay public. Oftentimes it is the amazing stories of
how animals adapt to their environments that capture the imagination and enthusiasm of non-scientists, including elected officials, and enhance their appreciation and support for basic research. The comparative reviews published in Physiology are an excellent means of transmitting those stories beyond the laboratory and the field, and into the hands of people in the “real world.” 䡲 No conflicts of interest, financial or otherwise, are declared by the author(s).
References 1.
Carey HV, Martin SL, Horwitz BA, Yan L, Bailey SM, Podrabsky J, Storz JF, Ortiz RM, Wong RP, Lathrop DA. Elucidating nature’s solutions to heart, lung, and blood diseases and sleep disorders. Circ Res 110: 915–921, 2012.
2.
Doherty AH, Ghalambor CK, Donahue SW. Evolutionary physiology of bone: bone metabolism in changing environments. Physiology 30: 17–29, 2015.
3.
Fuller A, Hetem RS, Maloney SK, Mitchell D. Adaptation to heat and water shortage in large, arid-zone mammals. Physiology 29: 159 –167, 2014.
4.
Harrison JF, Waters JS, Cease AJ, Vandenbrooks JM, Callier V, Klok CJ, Shaffer K, Socha JJ. How locusts breathe. Physiology 28: 18 –27, 2013.
5.
Kultz D. The combinatorial nature of osmosensing in fishes. Physiology 27: 259 –275, 2012.
6.
Madsen PT, Surlykke A. Functional convergence in bat and toothed whale biosonars. Physiology 28: 276 –283, 2013.
7.
Maloney SK, Fuller A, Mitchell D, Gordon C, Overton JM. Translating animal model research: does it matter that our rodents are cold? Physiology 29: 413– 420, 2014.
8.
Panneton WM. The mammalian diving response: an enigmatic reflex to preserve life? Physiology 28: 284 –297, 2013.
9.
Price ER, Brun A, Caviedes-Vidal E, Karasov WH. Digestive adaptations of aerial lifestyles. Physiology 30: 69 –78, 2015.
10. Williams CT, Barnes BM, Buck CL. Persistence, entrainment, and function of circadian rhythms in polar vertebrates. Physiology 30: 86 –96, 2015.
PHYSIOLOGY • Volume 30 • March 2015 • www.physiologyonline.org
81
Downloaded from on March 18, 2015
abolic rate required to maintain thermal neutrality in laboratory mice housed below their lower critical temperature (less than ⬃30°C) can have significant effects on physiology, morphology, and immunology throughout the body, thus potentially affecting the outcomes of experimental manipulations. One lesson we might take home from this is that communication and collaboration between biomedical scientists and comparative physiologists can potentially improve and enhance research that uses conventional laboratory animals and may also lead to greater incorporation of nonconventional species into the biomedical toolbox. Many of the authors of these comparative physiology reviews have pointed out the importance of technological advances that have enabled collection and analysis of data crucial for major advances in the field, sometimes overturning long-held views that were developed in their absence. The study of insect breathing has benefited greatly from use of synchrotron X-ray phase contrast imaging to understand the relative roles of diffusive vs. convective gas transport (4). By incorporating the complexity of the soundscape and the behavior of animals in the field, developments in tagging and recording technology have greatly expanded what was known from laboratory research on biosonar systems in bats and toothed whales (6). Biologging technology is increasing our understanding of the mechanisms and ecological relevance of physiological systems of diverse species. For example, loggers that track body temperature and heart rate in free-living an-
Physiology 30:80-81, 2015. doi:10.1152/physiol.00003.2015 You might find this additional info useful... This article cites 10 articles, 10 of which can be accessed free at: /content/30/2/80.full.html#ref-list-1 Updated information and services including high resolution figures, can be found at: /content/30/2/80.full.html Additional material and information about Physiology can be found at: http://www.the-aps.org/publications/physiol
This information is current as of March 18, 2015.
Downloaded from on March 18, 2015
Physiology (formerly published as News in Physiological Science) publishes brief review articles on major physiological developments. It is published bimonthly in January, March, May, July, September, and November by the American Physiological Society, 9650 Rockville Pike, Bethesda, MD 20814-3991. Copyright © 2015 by the American Physiological Society. ISSN: 1548-9213, ESSN: 1548-9221. Visit our website at http://www.the-aps.org/.
PHYSIOLOGY’S IMPACT
Hannah V. Carey University of Wisconsin-Madison, Madison, Wisconsin
PHYSIOLOGY 30: 80 – 81, 2015; doi:10.1152/physiol.00003.2015
Lessons Learned From Comparative and Evolutionary Physiology
80
echolocating bats and toothed whales, a stunning example of how evolution produced a remarkable level of similarity in the sensing of prey with ultrasound in two disparate animal groups Despite their extreme differences in size (very large, very small) and environment (water and air), bats and toothed whales use similar call frequencies and acoustic behavior while foraging in dark environments. In a similar vein, Price and colleagues (9) explain how the relatively smaller intestines of flying birds and bats, a trait likely driven by the selective pressure to reduce body mass to overcome gravity, constrains the capacity for digestion and absorption. Recent studies suggest both birds and bats compensate by having higher amplification of their intestinal villi and by having relatively high rates of paracellular as opposed to transcellular, transporter-mediated nutrient absorption. The selective pressures of aerial lifestyles were apparently solved in quite similar ways in these two vertebrate classes. Diversity in mechanisms of oxygen uptake and distribution in two animal phyla are described by Panneton (8) and Harrison et al. (4). The comparative approach has led to in-depth understanding of the mechanics of the diving response, a reflex that is found in all vertebrates but is most well developed in aquatic species (8). This combination of three independent reflexes that enhance survival in low-oxygen conditions involves redistribution of blood flow through peripheral vasoconstriction, such that oxygenated blood is directed preferentially to the central nervous system and heart at the expense of cutaneous, muscular, and splanchnic circulations. Oxygen uptake in insects is ancient and elaborate, and differs substantially from mammalian systems, with greater capacity for oxygen delivery from air to cells by either diffusive or convective mechanisms, and marked differences in morphological and structural components (4). Knowledge of these highly successful insect fluidic sys-
1548-9213/15 ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc.
Downloaded from on March 18, 2015
Comparative physiology is the exploration of physiological principles through examination of the functional diversity among animal species. Because diversity derives from evolution and natural selection, the work comparative physiologists do often extends beyond characterizing a physiological system at the mechanistic level to consideration of how the mechanism is relevant in an ecological or evolutionary context. One of the major goals of the field is to determine what ecological pressures have led to a particular physiological adaptation having a selective advantage, and how selective pressures have produced the differences (and similarities) we see among different species. For the most part, comparative physiologists choose study animals that diverge from the conventional laboratory species, with the gold standard being the ability to study physiology in free-living animals behaving in their natural environments. Thus the physiology underlying comparative studies tends to be more closely associated with responses to reallife challenges that are often not possible to replicate in the caged setting or in animals that have been bred for many generations to thrive in a caged environment where they are exposed to generic ambient housing conditions. Sometimes comparative physiology questions take this literally to the extreme by using species that live in highly challenging environments (e.g., deserts, high elevation, polar regions, deep oceans). Several recent articles published in Physiology highlight how comparative physiologists are identifying physiological solutions to ecological problems that have evolved in diverse groups of animals. They provide us with lessons to be learned on several fronts. Comparative approaches are particularly powerful when they reveal how fundamental ecological challenges have led to convergence in physiological pathways. Madsen and Surlykke (6) describe the convergence in biosonar systems in
tems can serve as bioinspiration for such fields a microfluidics, nanofabrication, and tissue engineering (4). Using comparative physiology to elucidate nature’s solutions to biomedical problems has a long history and is the foundation of the Krogh Principle (1). Although sometimes mentioned as a constraint for experimentation, the diverse genetic background of most species used in comparative physiology research makes these species very appropriate as animal models for human biomedical investigation. The heterogeneous natures of human populations in terms of genetics, epigenetic landscape, and the range of environmental factors that can affect physiology and health are more in tune to species that are living or are recently derived from wild populations, as opposed to conventional, laboratory-bred animals. Furthermore, the mechanisms by which certain animals thrive in environments we humans consider “extreme” can provide new avenues to pursue in the management of recalcitrant medical challenges. Many of the comparative reviews published in Physiology illustrate these principles very well. Understanding how and why skeletal systems evolved in diverse groups of vertebrates may provide new approaches for treatments of skeletal diseases, such as osteoporosis (2). The evolutionary and ecological bases for persistence or lack of circadian cycles in polar species may contribute to better treatment for circadian disorders in humans (10). Unraveling the complexity of osmoregulatory systems in fish may provide clues to treat fluid and electrolyte disorders (5). Identifying mechanisms that control the diving response can shed light on how the mammalian brain controls autonomic function and contributes to preservation of tissue oxygenation in nondiving species (8). Comparative physiology can also contribute to biomedical research by aiding the appropriate design of housing facilities for conventional laboratory animals. Maloney and colleagues (7) point out that inadequate understanding of an animal’s thermal biology can result in housing temperatures that, although comfortable for humans, are outside of the thermal neutral zone for the particular species. For example, the increased met-
imals, used in parallel with collars that monitor amount and type of light exposure, are helping to resolve why circadian rhythmicity in some polar vertebrates persists under conditions of continuous light or dark, but not in others (10). The importance of studying animal physiology in the field and the technology that supports field physiology are major themes of the review by Fuller et. al., who address adaptations to heat and water storage in large, arid-zone mammals (3). The ability to monitor both environmental and body temperatures in the wild where animals can select the microclimates they prefer has led to a new appreciation for “selective brain cooling” (SBC), which was long thought to be an important mechanism to protect the brain from hyperthermic damage in hot environments. In fact, biologging studies have shown that animals may abandon SBC during high-intensity exercise when brain temperatures climb as high as 42°C, perhaps to balance thermoregulatory and osmoregulatory needs. Research like this on free-ranging animals is needed to inform management decisions for species particularly vulnerable to changing environments, be they due to climate change, habitat destruction, or other anthropomorphic alterations to the planet. Beyond the generation of new knowledge and its potential application to fields like bioengineering and biomedicine, comparative physiology is enormously valuable in generating interest in animal biology in general, and physiology in particular, to students and the lay public. Oftentimes it is the amazing stories of
how animals adapt to their environments that capture the imagination and enthusiasm of non-scientists, including elected officials, and enhance their appreciation and support for basic research. The comparative reviews published in Physiology are an excellent means of transmitting those stories beyond the laboratory and the field, and into the hands of people in the “real world.” 䡲 No conflicts of interest, financial or otherwise, are declared by the author(s).
References 1.
Carey HV, Martin SL, Horwitz BA, Yan L, Bailey SM, Podrabsky J, Storz JF, Ortiz RM, Wong RP, Lathrop DA. Elucidating nature’s solutions to heart, lung, and blood diseases and sleep disorders. Circ Res 110: 915–921, 2012.
2.
Doherty AH, Ghalambor CK, Donahue SW. Evolutionary physiology of bone: bone metabolism in changing environments. Physiology 30: 17–29, 2015.
3.
Fuller A, Hetem RS, Maloney SK, Mitchell D. Adaptation to heat and water shortage in large, arid-zone mammals. Physiology 29: 159 –167, 2014.
4.
Harrison JF, Waters JS, Cease AJ, Vandenbrooks JM, Callier V, Klok CJ, Shaffer K, Socha JJ. How locusts breathe. Physiology 28: 18 –27, 2013.
5.
Kultz D. The combinatorial nature of osmosensing in fishes. Physiology 27: 259 –275, 2012.
6.
Madsen PT, Surlykke A. Functional convergence in bat and toothed whale biosonars. Physiology 28: 276 –283, 2013.
7.
Maloney SK, Fuller A, Mitchell D, Gordon C, Overton JM. Translating animal model research: does it matter that our rodents are cold? Physiology 29: 413– 420, 2014.
8.
Panneton WM. The mammalian diving response: an enigmatic reflex to preserve life? Physiology 28: 284 –297, 2013.
9.
Price ER, Brun A, Caviedes-Vidal E, Karasov WH. Digestive adaptations of aerial lifestyles. Physiology 30: 69 –78, 2015.
10. Williams CT, Barnes BM, Buck CL. Persistence, entrainment, and function of circadian rhythms in polar vertebrates. Physiology 30: 86 –96, 2015.
PHYSIOLOGY • Volume 30 • March 2015 • www.physiologyonline.org
81
Downloaded from on March 18, 2015
abolic rate required to maintain thermal neutrality in laboratory mice housed below their lower critical temperature (less than ⬃30°C) can have significant effects on physiology, morphology, and immunology throughout the body, thus potentially affecting the outcomes of experimental manipulations. One lesson we might take home from this is that communication and collaboration between biomedical scientists and comparative physiologists can potentially improve and enhance research that uses conventional laboratory animals and may also lead to greater incorporation of nonconventional species into the biomedical toolbox. Many of the authors of these comparative physiology reviews have pointed out the importance of technological advances that have enabled collection and analysis of data crucial for major advances in the field, sometimes overturning long-held views that were developed in their absence. The study of insect breathing has benefited greatly from use of synchrotron X-ray phase contrast imaging to understand the relative roles of diffusive vs. convective gas transport (4). By incorporating the complexity of the soundscape and the behavior of animals in the field, developments in tagging and recording technology have greatly expanded what was known from laboratory research on biosonar systems in bats and toothed whales (6). Biologging technology is increasing our understanding of the mechanisms and ecological relevance of physiological systems of diverse species. For example, loggers that track body temperature and heart rate in free-living an-
