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Basking behavior reveals vulnerability to climate change

Basking behavior reveals vulnerability to climate change © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 136-138 OUTSIDE JEB Glover and his colleagues found that the these primitive hypoxia heroes are not Hagfish pump some iron hagfish does take up iron through the skin ready to divulge all their secrets just yet; – and at a higher rate than in the gut. Also, they’ve got them clenched in an iron fist – over all but the highest iron concentrations, er, fin. the uptake in both tissue types initially 10.1242/jeb.147421 increased with concentration and then reached a plateau. In addition, most iron Glover, C. M., Niyogi, S., Blewitt, T. A. and Wood, C. M. (2016). Iron transport across the skin and gut absorbed by the skin remained in the skin, epithelia of Pacific hagfish: kinetic characterisation while iron absorbed by the gut tended to and effect of hypoxia. Comp. Biochem. Phys. A move across the tissue. The initial 199,1-7. increase and subsequent uptake plateau Molly H. B. Amador indicate that specific transporter University of Miami molecules are responsible for moving the [email protected] iron in both tissues (as these molecules at some point reach a maximum transport capacity). However, the discrepancy in The call of the not-so-mild transport rates and in the iron’s final destination suggests that each tissue handles iron differently. Along with other nutrients, animals need trace metals to function. Iron, the oxygen- To find out whether hagfish alter iron binding component in the blood pigment transport during hypoxia – when the hemoglobin, is a critical trace metal and is oxygen-binding metal is particularly usually absorbed through the gut. essential – the researchers again measured Mammals can alter iron metabolism in iron transport, but this time on skin and order to meet oxygen demand during gut from hagfish exposed to hypoxia for periods of low environmental oxygen – 24 h. They also analyzed the oxygen hypoxia. However, it was unknown content of the fish blood, the red blood whether hagfish – a much more primitive cell count and volume, the proportion of group of animals that exhibit unusual the blood made up of red blood cells and tolerance to hypoxia – change their iron the blood hemoglobin content to dynamics to achieve such resilience and determine whether hypoxia increases iron whether they could take up iron from their demand in hagfish as it does in mammals. environment. Knowing that hagfish can absorb some nutrients through their skin, Unexpectedly, hypoxia exposure did not Flies and many other insects show an Chris Glover, of Athabasca University, significantly change iron transport in inordinate fondness for feces. They Canada, and colleagues from several either the fish’s skin or gut. Also, unlike in oviposit there and occasionally visit other Canadian institutions set out to mammals, hypoxia did not appear to animal excrement to dine. But it turns out determine whether hagfish can take up increase iron demand in the blood. These that not all poop is created equal, and flies iron across the skin; if so, how it might results suggest that changes in iron are rather discerning in their choice of compare with gut uptake; and whether transport do not contribute to the hagfish’s fecal targets. While some piles of feces changes in iron transport during hypoxia outstanding hypoxia tolerance and that the are highly attractive, the fragrant bouquet contribute to the impressive hypoxia relative lack of change in blood of displeasing targets is met with extreme tolerance of these hardy fishes. parameters may preclude the need for prejudice. Now, in a recent paper in To begin to answer their questions, the any changes in iron transport in the first Current Biology, Suzan Mansourian and researchers measured iron transport across place. her collaborators from the University of the skin and gut tissue of Pacific hagfish. Lund in Sweden show why. Put simply, they exposed the external This study is the first to characterize trace surface of each tissue to a solution metal transport in hagfish skin or gut and Large mammals can be partitioned in containing radioactive iron at a range of to identify iron transport in hagfish skin. It many different ways, and one of the larger concentrations and measured how much also paves the way for future research by divisions concerns diet and the traits that radioactivity entered a saline solution on raising more questions: what is the nature go with it. Beyond the obvious differences the other side of the tissue after 2 h. They of the transporter; what happens to the between carnivores and herbivores (teeth, also measured how much radioactivity iron in hagfish skin; and is skin iron claws, etc.), these animals also differ in remained within the tissue itself. transport ancient or adaptive? Clearly, the length and structure of their guts. Outside JEB is a monthly feature that reports the most exciting developments in experimental biology. Articles that have been selected and written by a team of active research scientists highlight the papers that JEB readers can’t afford to miss. IRON TRANSPORT CHEMICAL ECOLOGY Journal of Experimental Biology OUTSIDE JEB Journal of Experimental Biology (2017) 220, 136-138 Deeper still, they maintain dramatically Does phenol concentration scale with the on the climate in their habitat, but on their different microbiomes to aid in digestion. true risk to flies? Are the phenol basking behavior, and highlights the high And it is this latter difference, according producers really pathogenic? I hope the vulnerability of ectothermic species to a to Mansourian and colleagues, that authors can address at least some of these warming climate. matters most to flies. intriguing questions in the future. The team first identified the thermal 10.1242/jeb.147173 When the research team offered flies a microhabitats and basking tendencies of choice between carnivore and herbivore seven lizard species by observing the Mansourian, S., Corcoran, J., Enjin, A., Lofstedt, C., Dacke, M. and Stensmyr, M. C. (2016). Fecal- feces for oviposition, they found marked animals in their natural environments and derived phenol induces egg-laying aversion in differences. While flies were attracted or measuring the temperatures of the surface Drosophila. Curr. Biol. 26, 2762-2769. indifferent to herbivore feces, they where the lizards were perching. They Daniel E. Rozen were positively repulsed by carnivore then collected lizards from the field and University of Leiden waste. Moreover, their aversion transferred them to the laboratory to [email protected] disappeared when the assays were repeated conduct a series of tests to classify the with flies lacking a specific type of physiological traits of each species. First, olfactory neuron, making it clear that their they flipped the lizards on their back at choice was caused by an odor preference. different temperatures and determined the Basking behavior reveals lowest and highest temperature at which vulnerability to climate To determine why one animal’s waste an individual was able to right itself. smelled better than the other, the team Following these tolerance tests, Muñoz change subjected the fecal samples to detailed and colleagues determined the thermal chemical analysis. It was little surprise sensitivity of sprinting speeds to establish that the feces contained a complex brew of the temperatures at which sprinting was smells. However, while many chemicals quickest for each species. distinguished feces in general from, say, a bottle of lager or a ripe banana, only very When the team analyzed the data, few were directly tied to the animal’s diet. including information on the Phenol, in particular, was abundant in phylogenetic relationship of the seven carnivore feces but entirely absent from species, they found that the basking the excrement of herbivores. More species were considerably more heat important, the team determined that this tolerant than the shade-seeking skinks. chemical alone was sufficient to drive fly Based on this observation, Muñoz and her behaviors. When normally acceptable colleagues concluded that the evolution of giraffe feces was spiked with phenol, the heat tolerance likely occurred when the flies turned up their noses and oviposited lizards specialized and selected either elsewhere. And when flies were forced to basking or shade-dwelling as their oviposit on phenol-laced food, they layed preferred lifestyle. They also suspect that nearly five times fewer eggs. this led to the differences that they found in heat tolerances even between lizards But why should flies avoid phenol? To Rising surface temperatures are that live in the same location. determine this, the team analyzed the threatening biodiversity worldwide, and Unfortunately, their finding that habitat bacteria found in herbivore and carnivore the impacts of climate change on temperature had no influence on heat guts. The most interesting differences, it organisms are hard to predict. tolerance also indicates that these turned out, were for bacterial species that Ectothermic species, such as lizards, rely species may not be able to adapt quickly are pathogenic for insects. And these to a large degree on environmental enough to match the pace of climate bacterial species, not coincidentally, temperatures to maintain their body warming. make phenol. But don’t trust just flies. temperatures and might therefore be When the team offered dung beetles, especially impacted by the predicted However, the lizards’ cold tolerance bonafide poo experts, a choice between changes. A team of international seems to be shaped mainly by their herbivore and carnivore feces, these too researchers led by Martha Muñoz, from habitat conditions. The researchers found chose the former. Thus, aversion to Duke University, USA, has compared the that all lizards, regardless of their phenol cues appears to be widespread. thermal behavior and physiological basking behavior, were more cold characteristics of seven lizard species tolerant when they inhabited cooler The neatest aspects of these results are the living in eight different locations and habitats. In the cold, animals have no diverse links between chemical ecology, elevations of an Australian rainforest other option than to adjust their neurobiology and animal behavior. But region in order to examine how basking physiology to cope better in chilly these same aspects also highlight the behavior and thermal habitat influence the conditions. Interestingly, lizards from loose threads that offer some promising evolution of thermal physiology such as lower elevations, and therefore warmer avenues for future research. Among these, heat tolerance. This extensive study, environments, sprinted optimally at why are frugivorous fruit flies so published in Evolution, suggests that the lower temperatures than lizards from discriminating about feces? How reliable ability of a lizard species to tolerate hot cooler areas. The authors concluded that a cue is phenol for the risk of fly disease? environments is dependent not so much at lower elevations, lizards have a greater THERMAL TOLERANCE Journal of Experimental Biology OUTSIDE JEB Journal of Experimental Biology (2017) 220, 136-138 risk of overheating and that the lower layer of biological gender, and you’re Using a technique called RNA-seq, optimal sprinting temperatures could be sure to have a unique individual: it’s Metzger identified and quantified caused by an alteration of the lizards’ fascinating to consider that much of what essentially all of the genes being activity patterns to avoid heat stress. defines us is determined long before expressed in the brains of the offspring. we’re born. That’s because environment He compared the gene expression data This study emphasizes the high and genes can interact to influence of male and female half-siblings against vulnerability of shade-specialist lizards critical processes such as brain the backdrop of ‘Mom’ and found that with low heat tolerance to climate change, development, and this shapes individuals maternal stress had a big effect on and suggests that even closely related through neuroplasticity. In humans, for neuroplasticity. Even more striking, species may differ substantially in example, if a mother is extremely Metzger also found that sons and their ability to tolerate increasing stressed during pregnancy, her baby is daughters of stressed mothers tended to temperatures. more likely to suffer from mental health have opposite changes in gene issues as an adult, and the nature of these expression, resulting in profoundly 10.1242/jeb.147181 effects are often sex-specific. But does different neural phenotypes. For the same hold true for egg-laying example, the expression of genes Munoz, M. M., Langham G. M., Brandley, M. C., Rosauer, D. F., Williams, S. E. and Moritz, C. animals, such as fish, where the eggs involved in cellular metabolism and (2016). Basking behavior predicts the evolution of develop outside of the mother’s protein synthesis increased in daughters heat tolerance in Australian rainforest lizards. ‘environment’? David Metzger and and decreased in sons of stressed Evolution 70, 2537-2549. Patricia Schulte, from the University of mothers; whereas the expression of Julia Nowack British Columbia in Canada, asked this genes for neural development and University of Veterinary Medicine Vienna question in their recent study published synapse formation increased in sons and [email protected] in Proceedings of the Royal Society B. decreased in daughters. And don’t forget They wanted to know what effect a that the main factor driving these mother fish’s experiences have on her changes – maternal stress – happened Mom shapes daughters’ offspring’s brains, and whether these while these fish were merely un- brains differently effects are different in sons and spawned eggs, and a whole year had daughters. passed since then. This study by Metzger and Schulte offers compelling evidence that even in egg-laying Metzger began his experiments by animals, environmental factors that stressing threespine sticklebacks. Over a occur at the earliest stages 2-week period, he chased and air- of development have a dramatic and exposed these fish for 1 min every day, unique effect on sons and daughters. So which increased their stress hormone neuroplasticity might just be one levels. He also left some fish word made up of six syllables, but undisturbed during these 2 weeks for his it adds up to some really exciting unstressed group. Metzger then made science! several half-sibling crosses, where he used sperm from the same unstressed 10.1242/jeb.147207 father fish to fertilize eggs from one Metzger, D. C. H. and Schulte, P. M. (2016). stressed and one unstressed mother fish. Maternal stress has divergent effects on gene These half-siblings differed only in their expression patterns in the brains of male and mother’s genes and her experiences. female threespine stickleback. Proc. R. Soc. B 283, 20161734. Metzger spent a full year carefully It’s no secret that who we are has a lot to raising the offspring under identical Sarah Alderman do with our parents (genes) and how we conditions before checking to see how University of Guelph [email protected] were raised (environment). Add on a their brains differed. MATERNAL IMPACT Journal of Experimental Biology http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Biology The Company of Biologists

Basking behavior reveals vulnerability to climate change

Julia, Nowack,
Journal of Experimental Biology , Volume 220 (2) – Jan 15, 2017
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© 2021 The Company of Biologists. All rights reserved.
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0022-0949
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1477-9145
DOI
10.1242/jeb.147181
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Abstract

© 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 136-138 OUTSIDE JEB Glover and his colleagues found that the these primitive hypoxia heroes are not Hagfish pump some iron hagfish does take up iron through the skin ready to divulge all their secrets just yet; – and at a higher rate than in the gut. Also, they’ve got them clenched in an iron fist – over all but the highest iron concentrations, er, fin. the uptake in both tissue types initially 10.1242/jeb.147421 increased with concentration and then reached a plateau. In addition, most iron Glover, C. M., Niyogi, S., Blewitt, T. A. and Wood, C. M. (2016). Iron transport across the skin and gut absorbed by the skin remained in the skin, epithelia of Pacific hagfish: kinetic characterisation while iron absorbed by the gut tended to and effect of hypoxia. Comp. Biochem. Phys. A move across the tissue. The initial 199,1-7. increase and subsequent uptake plateau Molly H. B. Amador indicate that specific transporter University of Miami molecules are responsible for moving the [email protected] iron in both tissues (as these molecules at some point reach a maximum transport capacity). However, the discrepancy in The call of the not-so-mild transport rates and in the iron’s final destination suggests that each tissue handles iron differently. Along with other nutrients, animals need trace metals to function. Iron, the oxygen- To find out whether hagfish alter iron binding component in the blood pigment transport during hypoxia – when the hemoglobin, is a critical trace metal and is oxygen-binding metal is particularly usually absorbed through the gut. essential – the researchers again measured Mammals can alter iron metabolism in iron transport, but this time on skin and order to meet oxygen demand during gut from hagfish exposed to hypoxia for periods of low environmental oxygen – 24 h. They also analyzed the oxygen hypoxia. However, it was unknown content of the fish blood, the red blood whether hagfish – a much more primitive cell count and volume, the proportion of group of animals that exhibit unusual the blood made up of red blood cells and tolerance to hypoxia – change their iron the blood hemoglobin content to dynamics to achieve such resilience and determine whether hypoxia increases iron whether they could take up iron from their demand in hagfish as it does in mammals. environment. Knowing that hagfish can absorb some nutrients through their skin, Unexpectedly, hypoxia exposure did not Flies and many other insects show an Chris Glover, of Athabasca University, significantly change iron transport in inordinate fondness for feces. They Canada, and colleagues from several either the fish’s skin or gut. Also, unlike in oviposit there and occasionally visit other Canadian institutions set out to mammals, hypoxia did not appear to animal excrement to dine. But it turns out determine whether hagfish can take up increase iron demand in the blood. These that not all poop is created equal, and flies iron across the skin; if so, how it might results suggest that changes in iron are rather discerning in their choice of compare with gut uptake; and whether transport do not contribute to the hagfish’s fecal targets. While some piles of feces changes in iron transport during hypoxia outstanding hypoxia tolerance and that the are highly attractive, the fragrant bouquet contribute to the impressive hypoxia relative lack of change in blood of displeasing targets is met with extreme tolerance of these hardy fishes. parameters may preclude the need for prejudice. Now, in a recent paper in To begin to answer their questions, the any changes in iron transport in the first Current Biology, Suzan Mansourian and researchers measured iron transport across place. her collaborators from the University of the skin and gut tissue of Pacific hagfish. Lund in Sweden show why. Put simply, they exposed the external This study is the first to characterize trace surface of each tissue to a solution metal transport in hagfish skin or gut and Large mammals can be partitioned in containing radioactive iron at a range of to identify iron transport in hagfish skin. It many different ways, and one of the larger concentrations and measured how much also paves the way for future research by divisions concerns diet and the traits that radioactivity entered a saline solution on raising more questions: what is the nature go with it. Beyond the obvious differences the other side of the tissue after 2 h. They of the transporter; what happens to the between carnivores and herbivores (teeth, also measured how much radioactivity iron in hagfish skin; and is skin iron claws, etc.), these animals also differ in remained within the tissue itself. transport ancient or adaptive? Clearly, the length and structure of their guts. Outside JEB is a monthly feature that reports the most exciting developments in experimental biology. Articles that have been selected and written by a team of active research scientists highlight the papers that JEB readers can’t afford to miss. IRON TRANSPORT CHEMICAL ECOLOGY Journal of Experimental Biology OUTSIDE JEB Journal of Experimental Biology (2017) 220, 136-138 Deeper still, they maintain dramatically Does phenol concentration scale with the on the climate in their habitat, but on their different microbiomes to aid in digestion. true risk to flies? Are the phenol basking behavior, and highlights the high And it is this latter difference, according producers really pathogenic? I hope the vulnerability of ectothermic species to a to Mansourian and colleagues, that authors can address at least some of these warming climate. matters most to flies. intriguing questions in the future. The team first identified the thermal 10.1242/jeb.147173 When the research team offered flies a microhabitats and basking tendencies of choice between carnivore and herbivore seven lizard species by observing the Mansourian, S., Corcoran, J., Enjin, A., Lofstedt, C., Dacke, M. and Stensmyr, M. C. (2016). Fecal- feces for oviposition, they found marked animals in their natural environments and derived phenol induces egg-laying aversion in differences. While flies were attracted or measuring the temperatures of the surface Drosophila. Curr. Biol. 26, 2762-2769. indifferent to herbivore feces, they where the lizards were perching. They Daniel E. Rozen were positively repulsed by carnivore then collected lizards from the field and University of Leiden waste. Moreover, their aversion transferred them to the laboratory to [email protected] disappeared when the assays were repeated conduct a series of tests to classify the with flies lacking a specific type of physiological traits of each species. First, olfactory neuron, making it clear that their they flipped the lizards on their back at choice was caused by an odor preference. different temperatures and determined the Basking behavior reveals lowest and highest temperature at which vulnerability to climate To determine why one animal’s waste an individual was able to right itself. smelled better than the other, the team Following these tolerance tests, Muñoz change subjected the fecal samples to detailed and colleagues determined the thermal chemical analysis. It was little surprise sensitivity of sprinting speeds to establish that the feces contained a complex brew of the temperatures at which sprinting was smells. However, while many chemicals quickest for each species. distinguished feces in general from, say, a bottle of lager or a ripe banana, only very When the team analyzed the data, few were directly tied to the animal’s diet. including information on the Phenol, in particular, was abundant in phylogenetic relationship of the seven carnivore feces but entirely absent from species, they found that the basking the excrement of herbivores. More species were considerably more heat important, the team determined that this tolerant than the shade-seeking skinks. chemical alone was sufficient to drive fly Based on this observation, Muñoz and her behaviors. When normally acceptable colleagues concluded that the evolution of giraffe feces was spiked with phenol, the heat tolerance likely occurred when the flies turned up their noses and oviposited lizards specialized and selected either elsewhere. And when flies were forced to basking or shade-dwelling as their oviposit on phenol-laced food, they layed preferred lifestyle. They also suspect that nearly five times fewer eggs. this led to the differences that they found in heat tolerances even between lizards But why should flies avoid phenol? To Rising surface temperatures are that live in the same location. determine this, the team analyzed the threatening biodiversity worldwide, and Unfortunately, their finding that habitat bacteria found in herbivore and carnivore the impacts of climate change on temperature had no influence on heat guts. The most interesting differences, it organisms are hard to predict. tolerance also indicates that these turned out, were for bacterial species that Ectothermic species, such as lizards, rely species may not be able to adapt quickly are pathogenic for insects. And these to a large degree on environmental enough to match the pace of climate bacterial species, not coincidentally, temperatures to maintain their body warming. make phenol. But don’t trust just flies. temperatures and might therefore be When the team offered dung beetles, especially impacted by the predicted However, the lizards’ cold tolerance bonafide poo experts, a choice between changes. A team of international seems to be shaped mainly by their herbivore and carnivore feces, these too researchers led by Martha Muñoz, from habitat conditions. The researchers found chose the former. Thus, aversion to Duke University, USA, has compared the that all lizards, regardless of their phenol cues appears to be widespread. thermal behavior and physiological basking behavior, were more cold characteristics of seven lizard species tolerant when they inhabited cooler The neatest aspects of these results are the living in eight different locations and habitats. In the cold, animals have no diverse links between chemical ecology, elevations of an Australian rainforest other option than to adjust their neurobiology and animal behavior. But region in order to examine how basking physiology to cope better in chilly these same aspects also highlight the behavior and thermal habitat influence the conditions. Interestingly, lizards from loose threads that offer some promising evolution of thermal physiology such as lower elevations, and therefore warmer avenues for future research. Among these, heat tolerance. This extensive study, environments, sprinted optimally at why are frugivorous fruit flies so published in Evolution, suggests that the lower temperatures than lizards from discriminating about feces? How reliable ability of a lizard species to tolerate hot cooler areas. The authors concluded that a cue is phenol for the risk of fly disease? environments is dependent not so much at lower elevations, lizards have a greater THERMAL TOLERANCE Journal of Experimental Biology OUTSIDE JEB Journal of Experimental Biology (2017) 220, 136-138 risk of overheating and that the lower layer of biological gender, and you’re Using a technique called RNA-seq, optimal sprinting temperatures could be sure to have a unique individual: it’s Metzger identified and quantified caused by an alteration of the lizards’ fascinating to consider that much of what essentially all of the genes being activity patterns to avoid heat stress. defines us is determined long before expressed in the brains of the offspring. we’re born. That’s because environment He compared the gene expression data This study emphasizes the high and genes can interact to influence of male and female half-siblings against vulnerability of shade-specialist lizards critical processes such as brain the backdrop of ‘Mom’ and found that with low heat tolerance to climate change, development, and this shapes individuals maternal stress had a big effect on and suggests that even closely related through neuroplasticity. In humans, for neuroplasticity. Even more striking, species may differ substantially in example, if a mother is extremely Metzger also found that sons and their ability to tolerate increasing stressed during pregnancy, her baby is daughters of stressed mothers tended to temperatures. more likely to suffer from mental health have opposite changes in gene issues as an adult, and the nature of these expression, resulting in profoundly 10.1242/jeb.147181 effects are often sex-specific. But does different neural phenotypes. For the same hold true for egg-laying example, the expression of genes Munoz, M. M., Langham G. M., Brandley, M. C., Rosauer, D. F., Williams, S. E. and Moritz, C. animals, such as fish, where the eggs involved in cellular metabolism and (2016). Basking behavior predicts the evolution of develop outside of the mother’s protein synthesis increased in daughters heat tolerance in Australian rainforest lizards. ‘environment’? David Metzger and and decreased in sons of stressed Evolution 70, 2537-2549. Patricia Schulte, from the University of mothers; whereas the expression of Julia Nowack British Columbia in Canada, asked this genes for neural development and University of Veterinary Medicine Vienna question in their recent study published synapse formation increased in sons and [email protected] in Proceedings of the Royal Society B. decreased in daughters. And don’t forget They wanted to know what effect a that the main factor driving these mother fish’s experiences have on her changes – maternal stress – happened Mom shapes daughters’ offspring’s brains, and whether these while these fish were merely un- brains differently effects are different in sons and spawned eggs, and a whole year had daughters. passed since then. This study by Metzger and Schulte offers compelling evidence that even in egg-laying Metzger began his experiments by animals, environmental factors that stressing threespine sticklebacks. Over a occur at the earliest stages 2-week period, he chased and air- of development have a dramatic and exposed these fish for 1 min every day, unique effect on sons and daughters. So which increased their stress hormone neuroplasticity might just be one levels. He also left some fish word made up of six syllables, but undisturbed during these 2 weeks for his it adds up to some really exciting unstressed group. Metzger then made science! several half-sibling crosses, where he used sperm from the same unstressed 10.1242/jeb.147207 father fish to fertilize eggs from one Metzger, D. C. H. and Schulte, P. M. (2016). stressed and one unstressed mother fish. Maternal stress has divergent effects on gene These half-siblings differed only in their expression patterns in the brains of male and mother’s genes and her experiences. female threespine stickleback. Proc. R. Soc. B 283, 20161734. Metzger spent a full year carefully It’s no secret that who we are has a lot to raising the offspring under identical Sarah Alderman do with our parents (genes) and how we conditions before checking to see how University of Guelph [email protected] were raised (environment). Add on a their brains differed. MATERNAL IMPACT Journal of Experimental Biology

Journal

Journal of Experimental Biology – The Company of Biologists

Published: Jan 15, 2017

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