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"Hill, Geoffrey E."
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The biology of color
Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science , this issue p. eaan0221 Coloration mediates the relationship between an organism and its environment in important ways, including social signaling, antipredator defenses, parasitic exploitation, thermoregulation, and protection from ultraviolet light, microbes, and abrasion. Methodological breakthroughs are accelerating knowledge of the processes underlying both the production of animal coloration and its perception, experiments are advancing understanding of mechanism and function, and measurements of color collected noninvasively and at a global scale are opening windows to evolutionary dynamics more generally. Here we provide a roadmap of these advances and identify hitherto unrecognized challenges for this multi- and interdisciplinary field.
Journal Article
National Geographic bird coloration
Seventeen short chapters with engaging narrative and lots of photos with information-packed captions illustrate the mechanisms by which birds produce the characteristic and sometimes brilliant coloration of their feathers and other body parts.
Book
Carotenoid metabolism strengthens the link between feather coloration and individual quality
Thirty years of research has made carotenoid coloration a textbook example of an honest signal of individual quality, but tests of this idea are surprisingly inconsistent. Here, to investigate sources of this heterogeneity, we perform meta-analyses of published studies on the relationship between carotenoid-based feather coloration and measures of individual quality. To create color displays, animals use either carotenoids unchanged from dietary components or carotenoids that they biochemically convert before deposition. We hypothesize that converted carotenoids better reflect individual quality because of the physiological links between cellular function and carotenoid metabolism. We show that feather coloration is an honest signal of some, but not all, measures of quality. Where these relationships exist, we show that converted, but not dietary, carotenoid coloration drives the relationship. Our results have broad implications for understanding the evolutionary role of carotenoid coloration and the physiological mechanisms that maintain signal honesty of animal ornamental traits.
Studies of honest signaling have found an inconsistent relationship between carotenoid coloration and individual quality. Here, Weaver et al. compare dietary and biochemically converted carotenoid coloration using meta-analyses and show that converted carotenoids drive relationships with quality measures.
Journal Article
The Vitamin A–Redox Hypothesis: A Biochemical Basis for Honest Signaling via Carotenoid Pigmentation
Trade-offs in resource allocation have been widely stated as the means by which the honesty of ornamental traits is maintained, but an alternative to this resource trade-off hypothesis is that production of ornamentation is linked to the biochemical efficiency of vital cellular processes. Carotenoids are antioxidants, potentially tying carotenoid-based coloration to the oxidative state of an organism, and some carotenoids are also precursors for vitamin A, which regulates numerous cellular processes. We present a biochemical model for regulation of ornamental coloration based on interdependencies of carotenoid and retinoid biochemistry. We propose that vitamin A regulatory mechanisms, redox systems, and carotenoid pigmentation pathways link carotenoid coloration to oxidative state and to a host of important aspects of performance, such as immune function. The activity of β-carotene ketolase, which catalyzes the oxidation of yellow carotenoids into red carotenoids, is responsive to the states of vitamin A pools and redox systems such that coloration is a direct reflection of the physiological state of an animal. According to the vitamin A–redox hypothesis, feather coloration is associated with a range of performance measures because performance emerges from functionality of the same basic cellular processes that regulate pigmentation. We present the vitamin A–redox hypothesis as a testable alternative hypothesis to the resource trade-off hypothesis for the maintenance of honesty of carotenoid pigmentation.
Journal Article
Genetic hitchhiking, mitonuclear coadaptation, and the origins of mt DNA barcode gaps
DNA barcoding based on mitochondrial (mt) nucleotide sequences is an enigma. Neutral models of mt evolution predict DNA barcoding cannot work for recently diverged taxa, and yet, mt DNA barcoding accurately delimits species for many bilaterian animals. Meanwhile, mt DNA barcoding often fails for plants and fungi. I propose that because mt gene products must cofunction with nuclear gene products, the evolution of mt genomes is best understood with full consideration of the two environments that impose selective pressure on mt genes: the external environment and the internal genomic environment. Moreover, it is critical to fully consider the potential for adaptive evolution of not just protein products of mt genes but also of mt transfer RNAs and mt ribosomal RNAs. The tight linkage of genes on mt genomes that do not engage in recombination could facilitate selective sweeps whenever there is positive selection on any element in the mt genome, leading to the purging of mt genetic diversity within a population and to the rapid fixation of novel mt DNA sequences. Accordingly, the most important factor determining whether or not mt DNA sequences diagnose species boundaries may be the extent to which the mt chromosomes engage in recombination. Neutral models of mitochondrial evolution predict mitochondrial DNA barcoding cannot work for recently diverged taxa, but mt DNA barcoding accurately delimits species across a wide spectrum of bilaterian animals. I propose that the tight linkage of genes on mt genomes that do not engage in recombination could facilitate selective sweeps whenever there is positive selection on any element in the mt genome, leading to the purging of mt genetic diversity within a population and to the rapid fixation of novel mt DNA sequences. If selective sweeps play a key role in generating mt DNA barcode gaps, then the most important factor determining whether or not mt DNA sequences diagnose species boundaries within a taxon would be the extent to which the mt chromosomes of individuals within that taxon engage in recombination.
Journal Article
Sexiness, Individual Condition, and Species Identity: The Information Signaled by Ornaments and Assessed by Choosing Females
Biologists have long debated the evolution of animal ornamentation via female choice. Much of the discussion of ornament evolution has focused on three hypotheses: the species recognition hypothesis, the indicator trait hypothesis, and the runaway sexual selection hypothesis. These models of sexual selection have generally been considered in isolation, with each assessed as a potential complete explanation for ornament evolution. In fact, any choosing female potentially benefits by assessing three distinct characteristics of a prospective mate—species identity, individual condition, and sexiness—such that there can be no comprehensive explanation of ornamentation without consideration of the need for females to assess these three key attributes of males. There is no logical basis for advocating for the importance of one of these classes of information over another. Consideration that all three assessments of prospective males work in tandem to shape the evolution of female preferences for male ornaments leads to a better understanding of the diversity of ornamentation within and among animal species.
Journal Article
No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird
Dietary carotenoids have been proposed to boost immune system and antioxidant functions in vertebrate animals, but studies aimed at testing these physiological functions of carotenoids have often failed to find support. Here we subject yellow canaries (
Serinus canaria
), which possess high levels of carotenoids in their tissue, and white recessive canaries, which possess a knockdown mutation that results in very low levels of tissue carotenoids, to oxidative and pathogen challenges. Across diverse measures of physiological performance, we detect no differences between carotenoid-rich yellow and carotenoid-deficient white canaries. These results add further challenge to the assumption that carotenoids are directly involved in supporting physiological function in vertebrate animals. While some dietary carotenoids provide indirect benefits as retinoid precursors, our observations suggest that carotenoids themselves may play little to no direct role in key physiological processes in birds.
Dietary carotenoids have been proposed to have physiological benefits in addition to contributing to coloration. Here, Koch et al. compare immune and antioxidant functions in yellow, carotenoid-rich vs. white, carotenoid-deficient canaries and find no difference, suggesting a limited physiological role of carotenoids.
Journal Article
Mitonuclear Ecology
Eukaryotes were born of a chimeric union between two prokaryotes—the progenitors of the mitochondrial and nuclear genomes. Early in eukaryote evolution, most mitochondrial genes were lost or transferred to the nucleus, but a core set of genes that code exclusively for products associated with the electron transport system remained in the mitochondrion. The products of these mitochondrial genes work in intimate association with the products of nuclear genes to enable oxidative phosphorylation and core energy production. The need for coadaptation, the challenge of cotransmission, and the possibility of genomic conflict between mitochondrial and nuclear genes have profound consequences for the ecology and evolution of eukaryotic life. An emerging interdisciplinary field that I call “mitonuclear ecology” is reassessing core concepts in evolutionary ecology including sexual reproduction, two sexes, sexual selection, adaptation, and speciation in light of the interactions of mitochondrial and nuclear genomes.
Journal Article
Flexibility underlies differences in mitochondrial respiratory performance between migratory and non-migratory White-crowned Sparrows (Zonotrichia leucophrys)
Migration is one of the most energy-demanding behaviors observed in birds. Mitochondria are the primary source of energy used to support these long-distance movements, yet how mitochondria meet the energetic demands of migration is scarcely studied. We quantified changes in mitochondrial respiratory performance in the White-crowned Sparrow (Zonotrichia leucophrys), which has a migratory and non-migratory subspecies. We hypothesized that the long-distance migratory Gambel’s subspecies (Z. l. gambelii) would show higher mitochondrial respiratory performance compared to the non-migratory Nuttall’s subspecies (Z. l. nuttalli). We sampled Gambel’s individuals during spring pre-migration, active fall migration, and a period with no migration or breeding (winter). We sampled Nuttall’s individuals during periods coinciding with fall migration and the winter period of Gambel’s annual cycle. Overall, Gambel’s individuals had higher citrate synthase, a proxy for mitochondrial volume, than Nuttall’s individuals. This was most pronounced prior to and during migration. We found that both OXPHOS capacity (state 3) and basal respiration (state 4) of mitochondria exhibit high seasonal flexibility within Gambel’s individuals, with values highest during active migration. These values in Nuttall’s individuals were most similar to Gambel’s individuals in winter. Our observations indicate that seasonal changes in mitochondrial respiration play a vital role in migration energetics.
Journal Article