呼吁整合色素的非视觉功能及其与视觉功能的相互作用,以了解全球变化对视觉系统的影响

IF 4.6 1区 环境科学与生态学 Q1 ECOLOGY Functional Ecology Pub Date : 2024-09-18 DOI:10.1111/1365-2435.14656
Beth A. Reinke, Julian D. Avery, Jessica Hua
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Importantly, animal coloration, which derives from diverse pigments and structures and is shaped by numerous biotic and abiotic factors, occurs in both integumentary structures (i.e. skin, fur, feathers, beaks, scales and shells), and non-integumentary structures (i.e. inner organs and blood; Hill &amp; McGraw, <span>2006</span>). Because integumentary structures are the component that interacts directly with the environment, this is the tissue that is most likely to have an impact on the evolution of visual systems and is thus the focus of this perspective. To date, substantial progress has been made on our understanding of how organisms detect visual cues including the precise estimations of colour vision and visual capabilities (e.g. Maia et al., <span>2019</span>; van den Berg et al., <span>2020</span>; Vorobyev &amp; Osorio, <span>1998</span>) and how specific visual systems may be influenced by their environments (e.g. Endler, <span>1992</span>; Härer et al., <span>2018</span>; Leal &amp; Fleishman, <span>2002</span>). However, given the range of pigmented integumentary tissues that occur in nature (Figure 1), there is still much to learn about the non-visual functional significance of these pigments and how they may subsequently influence visual systems, particularly as global change alters selective landscapes (Koneru &amp; Caro, <span>2022</span>; Rojas, <span>2016</span>).</p>\n<figure><picture>\n<source media=\"(min-width: 1650px)\" srcset=\"/cms/asset/94a9c412-9249-4738-af22-4d7536a95a5b/fec14656-fig-0001-m.jpg\"/><img alt=\"Details are in the caption following the image\" data-lg-src=\"/cms/asset/94a9c412-9249-4738-af22-4d7536a95a5b/fec14656-fig-0001-m.jpg\" loading=\"lazy\" src=\"/cms/asset/8f3c678a-dc9e-4d42-a7f2-aa2c9bbe2ad9/fec14656-fig-0001-m.png\" title=\"Details are in the caption following the image\"/></picture><figcaption>\n<div><strong>FIGURE 1<span style=\"font-weight:normal\"></span></strong><div>Open in figure viewer<i aria-hidden=\"true\"></i><span>PowerPoint</span></div>\n</div>\n<div>Pigments are used to make the wide variety of animal coloration displayed here. Pigments used for signals have to date been given the most attention for the likely impacts of global change on their display. However, many of the pigments above actually have non-visual or unknown functions. (a) The function of the low and high melanin concentrations in the, respectively, light and dark polymorphs of these timber rattlesnakes (<i>Crotalus horridus</i>) are unknown. (b) The dark melanins of the wood tiger moth (<i>Parasemia plantaginis</i>) aid in thermoregulation but reduce the warning signal created by the contrast between melanins and the yellow colour. (c) The barred owl (<i>Strix varia</i>) feather has melanized (dark) and un-pigmented (white) sections. (d) The bright red skin of the northern red salamander (<i>Pseudotriton ruber</i>) advertises its toxicity as a part of a Müllerian mimicry group. (e) The blue colour created by biliverdin in these eastern blue bird (<i>Sialia sialis</i>) eggs is hypothesized to have a thermoregulatory function in some species because biliverdin reflects near infrared wavelengths. (f) The seemingly obvious orange morph of the brown anole (<i>Anolis sagrei</i>) is more cryptic than the brown morph to bird predators. (g) The orange belly of the harlequin toad (<i>Atelopus aff. franciscus</i>) has an unknown function. (h) The bright orange colours on the plastron of the painted turtle (<i>Chrysemys picta</i>) are attributed to stored carotenoids that may be moved into the bloodstream to counteract oxidative stress during recovery from overwintering stress. (i) The pigmented bib and mask of the common yellowthroat (<i>Geothlypis trichas</i>) are used as signals to advertise quality. Photo credits: Julian Avery (a, c, d, e, i), Beth Reinke (f, h), Bibiana Rojas (g), Wikimedia Commons (b: Charles J. Sharp).</div>\n</figcaption>\n</figure>\n<p>As human impacts increase, natural ecosystems are expected to face a diversity of pressures associated with environmental change (i.e. pollutants and habitat alteration) that may influence pigmentation and coloration (Delhey &amp; Peters, <span>2017</span>; Koneru &amp; Caro, <span>2022</span>). Increased extreme temperature variability associated with global climate change may decouple coevolved pigment and pattern relationships leading to important functional and ecological consequences. For example, heat and cold shocks during butterfly development have been shown to uncouple pigments from pattern formation in adults, resulting in potentially maladaptive displays (Connahs et al., <span>2016</span>). Similarly, artificial light at night can change amphibian coloration and, importantly, the ability for some amphibian species to match their backgrounds (Horn et al., <span>2023</span>). An important limitation in our understanding of how environmental change influences visual ecology is that research tends to consider cases where colour is a trait that performs a known function, such as when it is used for communication, camouflage or thermoregulation (e.g. Delhey &amp; Peters, <span>2017</span>; Zimova et al., <span>2016</span>). In these cases, selective pressures act directly on coloration (Figure 2). In contrast, while relevant to animal fitness and survival, the effects of the environmental change on pigments with functions such as antioxidation, support and physical protection have rarely been considered. The physiology, complex nature and functional obscurity of many pigments often prevent evolutionary ecologists from incorporating this information into studies of coloration. In this perspective piece, we argue for the need to consider the myriad functions of pigments themselves when making predictions about species' responses to global change, and the subsequent impacts on visual systems, because the functional significance of the pigment will determine which traits selection affects (Figure 2). Despite the past research bias towards visually adaptive signals, it is important to acknowledge that there are likely many unknown non-visual roles and synergistic effects of pigments involved in organismal responses to global change.</p>\n<figure><picture>\n<source media=\"(min-width: 1650px)\" srcset=\"/cms/asset/ad785f19-ac70-43de-811e-f025d458985b/fec14656-fig-0002-m.jpg\"/><img alt=\"Details are in the caption following the image\" data-lg-src=\"/cms/asset/ad785f19-ac70-43de-811e-f025d458985b/fec14656-fig-0002-m.jpg\" loading=\"lazy\" src=\"/cms/asset/0a97feab-8496-4efb-99bd-6ee9a2d5fee3/fec14656-fig-0002-m.png\" title=\"Details are in the caption following the image\"/></picture><figcaption>\n<div><strong>FIGURE 2<span style=\"font-weight:normal\"></span></strong><div>Open in figure viewer<i aria-hidden=\"true\"></i><span>PowerPoint</span></div>\n</div>\n<div>Theoretical framework illustrating how global change can impact colour and visual system evolution. Coloration can be made by pigments (specific biomolecules), structure (tissue that differentially reflect wavelengths of light) or a combination of the two. Selection will act on coloration in cases where the colour is used for communication, camouflage or thermoregulation and will act directly on pigments when the pigments are used for antioxidation, detoxification, structural support or protection. The strength and direction of the selective pressure on either or both traits may be altered by the modifiers. Changes to an organism's coloration will then impact the colour trait distribution of the ecosystem, which may also have impacts on visual systems of species within the ecosystem (intended receivers, predators, etc.).</div>\n</figcaption>\n</figure>\n<p>To address these gaps in our understanding of the functions of pigmentation and coloration, and their subsequent impacts on visual systems in the face of global change (defined as any human-induced environmental change), we will (1) summarize the main functions pigments can have in integument with a focus on non-visual roles, (2) provide an overview of how global change could impact coloration and pigmentation, (3) discuss some of the known modifiers between pigment functions and their interactions with global change and (4) connect these changes in colour traits to possible subsequent visual system evolution. Though both structural elements and pigments contribute to animal coloration (Figure 2), we focus here on pigments. Throughout this perspective, we highlight select examples that illustrate exciting directions in coloration research and where possible, we point the reader towards useful and insightful reviews.</p>","PeriodicalId":172,"journal":{"name":"Functional Ecology","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"A call to integrate non-visual functions of pigments and their interactions with visual functions to understand global change impacts on visual systems\",\"authors\":\"Beth A. Reinke, Julian D. Avery, Jessica Hua\",\"doi\":\"10.1111/1365-2435.14656\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<h2>1 INTRODUCTION</h2>\\n<p>Vision plays a central role in the ecology of many organisms, shaping the outcomes of their interactions with each other and the environment (e.g. predator–prey; host–parasite). The evolution of visual systems is impacted by variation in visual traits (e.g. coloration; Endler et al., <span>2005</span>), which can have signalling roles but which may also have <i>non-signalling functions</i> that have significant and synergistic effects (Koneru &amp; Caro, <span>2022</span>). Importantly, animal coloration, which derives from diverse pigments and structures and is shaped by numerous biotic and abiotic factors, occurs in both integumentary structures (i.e. skin, fur, feathers, beaks, scales and shells), and non-integumentary structures (i.e. inner organs and blood; Hill &amp; McGraw, <span>2006</span>). Because integumentary structures are the component that interacts directly with the environment, this is the tissue that is most likely to have an impact on the evolution of visual systems and is thus the focus of this perspective. To date, substantial progress has been made on our understanding of how organisms detect visual cues including the precise estimations of colour vision and visual capabilities (e.g. Maia et al., <span>2019</span>; van den Berg et al., <span>2020</span>; Vorobyev &amp; Osorio, <span>1998</span>) and how specific visual systems may be influenced by their environments (e.g. Endler, <span>1992</span>; Härer et al., <span>2018</span>; Leal &amp; Fleishman, <span>2002</span>). However, given the range of pigmented integumentary tissues that occur in nature (Figure 1), there is still much to learn about the non-visual functional significance of these pigments and how they may subsequently influence visual systems, particularly as global change alters selective landscapes (Koneru &amp; Caro, <span>2022</span>; Rojas, <span>2016</span>).</p>\\n<figure><picture>\\n<source media=\\\"(min-width: 1650px)\\\" srcset=\\\"/cms/asset/94a9c412-9249-4738-af22-4d7536a95a5b/fec14656-fig-0001-m.jpg\\\"/><img alt=\\\"Details are in the caption following the image\\\" data-lg-src=\\\"/cms/asset/94a9c412-9249-4738-af22-4d7536a95a5b/fec14656-fig-0001-m.jpg\\\" loading=\\\"lazy\\\" src=\\\"/cms/asset/8f3c678a-dc9e-4d42-a7f2-aa2c9bbe2ad9/fec14656-fig-0001-m.png\\\" title=\\\"Details are in the caption following the image\\\"/></picture><figcaption>\\n<div><strong>FIGURE 1<span style=\\\"font-weight:normal\\\"></span></strong><div>Open in figure viewer<i aria-hidden=\\\"true\\\"></i><span>PowerPoint</span></div>\\n</div>\\n<div>Pigments are used to make the wide variety of animal coloration displayed here. 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(e) The blue colour created by biliverdin in these eastern blue bird (<i>Sialia sialis</i>) eggs is hypothesized to have a thermoregulatory function in some species because biliverdin reflects near infrared wavelengths. (f) The seemingly obvious orange morph of the brown anole (<i>Anolis sagrei</i>) is more cryptic than the brown morph to bird predators. (g) The orange belly of the harlequin toad (<i>Atelopus aff. franciscus</i>) has an unknown function. (h) The bright orange colours on the plastron of the painted turtle (<i>Chrysemys picta</i>) are attributed to stored carotenoids that may be moved into the bloodstream to counteract oxidative stress during recovery from overwintering stress. (i) The pigmented bib and mask of the common yellowthroat (<i>Geothlypis trichas</i>) are used as signals to advertise quality. Photo credits: Julian Avery (a, c, d, e, i), Beth Reinke (f, h), Bibiana Rojas (g), Wikimedia Commons (b: Charles J. Sharp).</div>\\n</figcaption>\\n</figure>\\n<p>As human impacts increase, natural ecosystems are expected to face a diversity of pressures associated with environmental change (i.e. pollutants and habitat alteration) that may influence pigmentation and coloration (Delhey &amp; Peters, <span>2017</span>; Koneru &amp; Caro, <span>2022</span>). Increased extreme temperature variability associated with global climate change may decouple coevolved pigment and pattern relationships leading to important functional and ecological consequences. For example, heat and cold shocks during butterfly development have been shown to uncouple pigments from pattern formation in adults, resulting in potentially maladaptive displays (Connahs et al., <span>2016</span>). Similarly, artificial light at night can change amphibian coloration and, importantly, the ability for some amphibian species to match their backgrounds (Horn et al., <span>2023</span>). An important limitation in our understanding of how environmental change influences visual ecology is that research tends to consider cases where colour is a trait that performs a known function, such as when it is used for communication, camouflage or thermoregulation (e.g. Delhey &amp; Peters, <span>2017</span>; Zimova et al., <span>2016</span>). In these cases, selective pressures act directly on coloration (Figure 2). In contrast, while relevant to animal fitness and survival, the effects of the environmental change on pigments with functions such as antioxidation, support and physical protection have rarely been considered. The physiology, complex nature and functional obscurity of many pigments often prevent evolutionary ecologists from incorporating this information into studies of coloration. In this perspective piece, we argue for the need to consider the myriad functions of pigments themselves when making predictions about species' responses to global change, and the subsequent impacts on visual systems, because the functional significance of the pigment will determine which traits selection affects (Figure 2). 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引用次数: 0

摘要

相比之下,环境变化对具有抗氧化、支持和物理保护等功能的色素的影响虽然与动物的适应性和生存有关,但却很少被考虑。许多色素的生理学特性、复杂性和功能模糊性往往阻碍了进化生态学家将这些信息纳入着色研究。在这篇观点文章中,我们认为在预测物种对全球变化的反应以及随后对视觉系统的影响时,有必要考虑色素本身的多种功能,因为色素的功能意义将决定选择影响哪些性状(图 2)。尽管过去的研究偏重于视觉适应性信号,但重要的是要承认,在生物体对全球变化的反应中,可能还有许多未知的非视觉作用和色素的协同效应。颜色可由色素(特定生物分子)、结构(可反射不同波长光线的组织)或二者结合形成。当颜色用于交流、伪装或体温调节时,选择就会作用于色素;当色素用于抗氧化、解毒、结构支持或保护时,选择就会直接作用于色素。改良剂可能会改变对任一性状或两种性状的选择压力的强度和方向。生物体颜色的变化将影响生态系统的颜色性状分布,这也可能对生态系统内物种(目标接收者、捕食者等)的视觉系统产生影响。为了弥补我们对色素和着色的功能及其在全球变化(指任何由人类引起的环境变化)情况下对视觉系统的影响的认识上的差距,我们将:(1)总结色素在整体中的主要功能,重点是非视觉作用;(2)概述全球变化如何影响着色和色素沉着;(3)讨论色素功能之间的一些已知调节因素及其与全球变化的相互作用;(4)将这些颜色特征的变化与随后可能发生的视觉系统进化联系起来。虽然结构元素和色素都有助于动物着色(图 2),但我们在此重点讨论色素。在本视角中,我们将重点举例说明着色研究中令人兴奋的方向,并在可能的情况下为读者提供有用和有见地的综述。
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A call to integrate non-visual functions of pigments and their interactions with visual functions to understand global change impacts on visual systems

1 INTRODUCTION

Vision plays a central role in the ecology of many organisms, shaping the outcomes of their interactions with each other and the environment (e.g. predator–prey; host–parasite). The evolution of visual systems is impacted by variation in visual traits (e.g. coloration; Endler et al., 2005), which can have signalling roles but which may also have non-signalling functions that have significant and synergistic effects (Koneru & Caro, 2022). Importantly, animal coloration, which derives from diverse pigments and structures and is shaped by numerous biotic and abiotic factors, occurs in both integumentary structures (i.e. skin, fur, feathers, beaks, scales and shells), and non-integumentary structures (i.e. inner organs and blood; Hill & McGraw, 2006). Because integumentary structures are the component that interacts directly with the environment, this is the tissue that is most likely to have an impact on the evolution of visual systems and is thus the focus of this perspective. To date, substantial progress has been made on our understanding of how organisms detect visual cues including the precise estimations of colour vision and visual capabilities (e.g. Maia et al., 2019; van den Berg et al., 2020; Vorobyev & Osorio, 1998) and how specific visual systems may be influenced by their environments (e.g. Endler, 1992; Härer et al., 2018; Leal & Fleishman, 2002). However, given the range of pigmented integumentary tissues that occur in nature (Figure 1), there is still much to learn about the non-visual functional significance of these pigments and how they may subsequently influence visual systems, particularly as global change alters selective landscapes (Koneru & Caro, 2022; Rojas, 2016).

Details are in the caption following the image
FIGURE 1
Open in figure viewerPowerPoint
Pigments are used to make the wide variety of animal coloration displayed here. Pigments used for signals have to date been given the most attention for the likely impacts of global change on their display. However, many of the pigments above actually have non-visual or unknown functions. (a) The function of the low and high melanin concentrations in the, respectively, light and dark polymorphs of these timber rattlesnakes (Crotalus horridus) are unknown. (b) The dark melanins of the wood tiger moth (Parasemia plantaginis) aid in thermoregulation but reduce the warning signal created by the contrast between melanins and the yellow colour. (c) The barred owl (Strix varia) feather has melanized (dark) and un-pigmented (white) sections. (d) The bright red skin of the northern red salamander (Pseudotriton ruber) advertises its toxicity as a part of a Müllerian mimicry group. (e) The blue colour created by biliverdin in these eastern blue bird (Sialia sialis) eggs is hypothesized to have a thermoregulatory function in some species because biliverdin reflects near infrared wavelengths. (f) The seemingly obvious orange morph of the brown anole (Anolis sagrei) is more cryptic than the brown morph to bird predators. (g) The orange belly of the harlequin toad (Atelopus aff. franciscus) has an unknown function. (h) The bright orange colours on the plastron of the painted turtle (Chrysemys picta) are attributed to stored carotenoids that may be moved into the bloodstream to counteract oxidative stress during recovery from overwintering stress. (i) The pigmented bib and mask of the common yellowthroat (Geothlypis trichas) are used as signals to advertise quality. Photo credits: Julian Avery (a, c, d, e, i), Beth Reinke (f, h), Bibiana Rojas (g), Wikimedia Commons (b: Charles J. Sharp).

As human impacts increase, natural ecosystems are expected to face a diversity of pressures associated with environmental change (i.e. pollutants and habitat alteration) that may influence pigmentation and coloration (Delhey & Peters, 2017; Koneru & Caro, 2022). Increased extreme temperature variability associated with global climate change may decouple coevolved pigment and pattern relationships leading to important functional and ecological consequences. For example, heat and cold shocks during butterfly development have been shown to uncouple pigments from pattern formation in adults, resulting in potentially maladaptive displays (Connahs et al., 2016). Similarly, artificial light at night can change amphibian coloration and, importantly, the ability for some amphibian species to match their backgrounds (Horn et al., 2023). An important limitation in our understanding of how environmental change influences visual ecology is that research tends to consider cases where colour is a trait that performs a known function, such as when it is used for communication, camouflage or thermoregulation (e.g. Delhey & Peters, 2017; Zimova et al., 2016). In these cases, selective pressures act directly on coloration (Figure 2). In contrast, while relevant to animal fitness and survival, the effects of the environmental change on pigments with functions such as antioxidation, support and physical protection have rarely been considered. The physiology, complex nature and functional obscurity of many pigments often prevent evolutionary ecologists from incorporating this information into studies of coloration. In this perspective piece, we argue for the need to consider the myriad functions of pigments themselves when making predictions about species' responses to global change, and the subsequent impacts on visual systems, because the functional significance of the pigment will determine which traits selection affects (Figure 2). Despite the past research bias towards visually adaptive signals, it is important to acknowledge that there are likely many unknown non-visual roles and synergistic effects of pigments involved in organismal responses to global change.

Details are in the caption following the image
FIGURE 2
Open in figure viewerPowerPoint
Theoretical framework illustrating how global change can impact colour and visual system evolution. Coloration can be made by pigments (specific biomolecules), structure (tissue that differentially reflect wavelengths of light) or a combination of the two. Selection will act on coloration in cases where the colour is used for communication, camouflage or thermoregulation and will act directly on pigments when the pigments are used for antioxidation, detoxification, structural support or protection. The strength and direction of the selective pressure on either or both traits may be altered by the modifiers. Changes to an organism's coloration will then impact the colour trait distribution of the ecosystem, which may also have impacts on visual systems of species within the ecosystem (intended receivers, predators, etc.).

To address these gaps in our understanding of the functions of pigmentation and coloration, and their subsequent impacts on visual systems in the face of global change (defined as any human-induced environmental change), we will (1) summarize the main functions pigments can have in integument with a focus on non-visual roles, (2) provide an overview of how global change could impact coloration and pigmentation, (3) discuss some of the known modifiers between pigment functions and their interactions with global change and (4) connect these changes in colour traits to possible subsequent visual system evolution. Though both structural elements and pigments contribute to animal coloration (Figure 2), we focus here on pigments. Throughout this perspective, we highlight select examples that illustrate exciting directions in coloration research and where possible, we point the reader towards useful and insightful reviews.

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来源期刊
Functional Ecology
Functional Ecology 环境科学-生态学
CiteScore
9.00
自引率
1.90%
发文量
243
审稿时长
4 months
期刊介绍: Functional Ecology publishes high-impact papers that enable a mechanistic understanding of ecological pattern and process from the organismic to the ecosystem scale. Because of the multifaceted nature of this challenge, papers can be based on a wide range of approaches. Thus, manuscripts may vary from physiological, genetics, life-history, and behavioural perspectives for organismal studies to community and biogeochemical studies when the goal is to understand ecosystem and larger scale ecological phenomena. We believe that the diverse nature of our journal is a strength, not a weakness, and we are open-minded about the variety of data, research approaches and types of studies that we publish. Certain key areas will continue to be emphasized: studies that integrate genomics with ecology, studies that examine how key aspects of physiology (e.g., stress) impact the ecology of animals and plants, or vice versa, and how evolution shapes interactions among function and ecological traits. Ecology has increasingly moved towards the realization that organismal traits and activities are vital for understanding community dynamics and ecosystem processes, particularly in response to the rapid global changes occurring in earth’s environment, and Functional Ecology aims to publish such integrative papers.
期刊最新文献
Cover Picture and Issue Information Effects of warming and parasitism on root traits and the root economics space A call to integrate non-visual functions of pigments and their interactions with visual functions to understand global change impacts on visual systems Seasonal acclimation of photosynthetic thermal tolerances in six woody tropical species along a thermal gradient Host community structure can shape pathogen outbreak dynamics through a phylogenetic dilution effect
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