The carotenoid redshift: Physical basis and implications for visual signaling.

Carotenoid pigments are the basis for much red, orange, and yellow coloration in nature and central to visual signaling. However, as pigment concentration increases, carotenoid signals not only darken and become more saturated but they also redshift; for example, orange pigments can look red at higher concentration. This occurs because light experiences exponential attenuation, and carotenoid-based signals have spectrally asymmetric reflectance in the visible range. Adding pigment disproportionately affects the high-absorbance regions of the reflectance spectra, which redshifts the perceived hue. This carotenoid redshift is substantial and perceivable by animal observers. In addition, beyond pigment concentration, anything that increases the path length of light through pigment causes this redshift (including optical nano- and microstructures). For example, male Ramphocelus tanagers appear redder than females, despite the same population and concentration of carotenoids, due to microstructures that enhance light-pigment interaction. This mechanism of carotenoid redshift has sensory and evolutionary consequences for honest signaling in that structures that redshift carotenoid ornaments may decrease signal honesty. More generally, nearly all colorful signals vary in hue, saturation, and brightness as light-pigment interactions change, due to spectrally asymmetrical reflectance within the visible range of the relevant species. Therefore, the three attributes of color need to be considered together in studies of honest visual signaling.

Dead rats, dopamine, performance metrics, and peacock tails: proxy failure is an inherent risk in goal-oriented systems.

When a measure becomes a target, it ceases to be a good measure. For example, when standardized test scores in education become targets, teachers may start 'teaching to the test', leading to breakdown of the relationship between the measure--test performance--and the underlying goal--quality education. Similar phenomena have been named and described across a broad range of contexts, such as economics, academia, machine-learning, and ecology. Yet it remains unclear whether these phenomena bear only superficial similarities, or if they derive from some fundamental unifying mechanism. Here, we propose such a unifying mechanism, which we label proxy failure. We first review illustrative examples and their labels, such as the 'Cobra effect', 'Goodhart's law', and 'Campbell's law'. Second, we identify central prerequisites and constraints of proxy failure, noting that it is often only a partial failure or divergence. We argue that whenever incentivization or selection is based on an imperfect proxy measure of the underlying goal, a pressure arises which tends to make the proxy a worse approximation of the goal. Third, we develop this perspective for three concrete contexts, namely neuroscience, economics and ecology, highlighting similarities and differences. Fourth, we outline consequences of proxy failure, suggesting it is key to understanding the structure and evolution of goal-oriented systems. Our account draws on a broad range of disciplines, but we can only scratch the surface within each. We thus hope the present account elicits a collaborative enterprise, entailing both critical discussion as well as extensions in contexts we have missed.

Meiosis solved the problem of gerrymandering.

Gerrymandering, the structuring of voting districts to favour certain politicians and political groups, undermines fair elections and presents a serious challenge to democracy. We introduce a solution to gerrymandering inspired by the biological process of cell division in sexually reproducing organisms, meiosis, in which the boundaries of electorates are frequently redrawn by randomizing algorithms. By demonstrating the deep parallels between meiosis and John Rawls's concept of a 'veil of ignorance', we also show how one of the biggest threats to the integrity of meiosis-selfish genetic elements, genes that promote their own transmission at the expense of organismal fitness-can inspire another potential advantage to frequent random redistricting.

Species clustering, climate effects, and introduced species in 5 million city trees across 63 US cities.

Sustainable cities depend on urban forests. City trees-pillars of urban forests-improve our health, clean the air, store CO2, and cool local temperatures. Comparatively less is known about city tree communities as ecosystems, particularly regarding spatial composition, species diversity, tree health, and the abundance of introduced species. Here, we assembled and standardized a new dataset of N = 5,660,237 trees from 63 of the largest US cities with detailed information on location, health, species, and whether a species is introduced or naturally occurring (i.e., "native"). We further designed new tools to analyze spatial clustering and the abundance of introduced species. We show that trees significantly cluster by species in 98% of cities, potentially increasing pest vulnerability (even in species-diverse cities). Further, introduced species significantly homogenize tree communities across cities, while naturally occurring trees (i.e., "native" trees) comprise 0.51-87.4% (median = 45.6%) of city tree populations. Introduced species are more common in drier cities, and climate also shapes tree species diversity across urban forests. Parks have greater tree species diversity than urban settings. Compared to past work which focused on canopy cover and species richness, we show the importance of analyzing spatial composition and introduced species in urban ecosystems (and we develop new tools and datasets to do so). Future work could analyze city trees alongside sociodemographic variables or bird, insect, and plant diversity (e.g., from citizen-science initiatives). With these tools, we may evaluate existing city trees in new, nuanced ways and design future plantings to maximize resistance to pests and climate change. We depend on city trees.

Trees in towns and cities provide critical services to humans, animals and other living things. They help prevent climate change by capturing and storing carbon dioxide; they provide food and shelter to other species, they scrub the air of microscopic pollutants, cool local temperatures, and improve the mental and physical health of those who have access to them. In general, naturally occurring (so called native) plant species support richer local ecosystems ­ such as bird and butterfly communities ­ than plants that have been introduced from other areas. However, relatively little is known about which species of trees are found in towns and cities or how these species are distributed. Here, McCoy, Goulet-Scott et al. assembled a dataset of 5.6 million city trees from 63 cities in the United States. This dataset contained rich data on the exact location, species, and health of individual city trees ­ including park trees, those in urban forests, and trees that line city streets. In nearly all of the cities, the same tree species were found clustered next to each other, even in cities that had many different species of tree overall. This tendency of tree species to flock together may make these communities more vulnerable to disease and pest outbreaks. Trees in more developed environments, like those that line streets, were much less species diverse than trees spread across parks. Cities with wetter, cooler climates tended to have higher percentages of native tree species compared to cities with drier, hotter climates. Younger cities also had a greater percentage of native tree species than older cities, which may reflect increased awareness of the importance of native tree species among urban planners in more recent years. The cities that had planted non-native tree species tended to select the same species, which contributed to tree communities in different cities looking more alike. McCoy, Goulet-Scott et al. provide easy-to-use tools academics and urban foresters can use to assess how diverse tree communities in individual cities are. This work may help local decision-makers to select and plant trees that build resilience against climate change, pest and disease outbreaks, and maximize the health benefits trees provide all city dwellers.

After short interbirth intervals, captive callitrichine monkeys have higher infant mortality.

Life history theory predicts a trade-off between the quantity and quality of offspring. Short interbirth intervals-the time between successive births-may increase the quantity of offspring but harm offspring quality. In contrast, long interbirth intervals may bolster offspring quality while reducing overall reproductive output. Further research is needed to determine whether this relationship holds among primates, which have intensive parental investment. Using Cox proportional hazards models, we examined the effects of interbirth intervals (short, normal, or long) on infant survivorship using a large demographic dataset (n = 15,852) of captive callitrichine monkeys (marmosets, tamarins, and lion tamarins). In seven of the nine species studied, infants born after short interbirth intervals had significantly higher risks of mortality than infants born after longer interbirth intervals. These results suggest that reproduction in callitrichine primates may be limited by physiologic constraints, such that short birth spacing drives higher infant mortality.

Finite-difference Time-domain (FDTD) Optical Simulations: A Primer for the Life Sciences and Bio-Inspired Engineering.

Light influences most ecosystems on earth, from sun-dappled forests to bioluminescent creatures in the ocean deep. Biologists have long studied nano- and micro-scale organismal adaptations to manipulate light using ever-more sophisticated microscopy, spectroscopy, and other analytical equipment. In combination with experimental tools, simulations of light interacting with objects can help researchers determine the impact of observed structures and explore how variations affect optical function. In particular, the finite-difference time-domain (FDTD) method is widely used throughout the nanophotonics community to efficiently simulate light interacting with a variety of materials and optical devices. More recently, FDTD has been used to characterize optical adaptations in nature, such as camouflage in fish and other organisms, colors in sexually-selected birds and spiders, and photosynthetic efficiency in plants. FDTD is also common in bioengineering, as the design of biologically-inspired engineered structures can be guided and optimized through FDTD simulations. Parameter sweeps are a particularly useful application of FDTD, which allows researchers to explore a range of variables and modifications in natural and synthetic systems (e.g., to investigate the optical effects of changing the sizes, shape, or refractive indices of a structure). Here, we review the use of FDTD simulations in biology and present a brief methods primer tailored for life scientists, with a focus on the commercially available software Lumerical FDTD. We give special attention to whether FDTD is the right tool to use, how experimental techniques are used to acquire and import the structures of interest, and how their optical properties such as refractive index and absorption are obtained. This primer is intended to help researchers understand FDTD, implement the method to model optical effects, and learn about the benefits and limitations of this tool. Altogether, FDTD is well-suited to (i) characterize optical adaptations and (ii) provide mechanistic explanations; by doing so, it helps (iii) make conclusions about evolutionary theory and (iv) inspire new technologies based on natural structures.

Microstructures amplify carotenoid plumage signals in tanagers.

Brilliantly-colored birds are a model system for research into evolution and sexual selection. Red, orange, and yellow carotenoid-colored plumages have been considered honest signals of condition; however, sex differences in feather pigments and microstructures are not well understood. Here, we show that microstructures, rather than carotenoid pigments, seem to be a major driver of male-female color differences in the social, sexually-dimorphic tanager genus Ramphocelus. We comprehensively quantified feather (i) color (using spectrophotometry), (ii) pigments (using liquid chromatography-mass spectrometry (LC-MS)), and (iii) microstructures (using scanning electron microscopy (SEM) and finite-difference time-domain (FDTD) optical modeling). Males have significantly more saturated color patches than females. However, our exploratory analysis of pigments suggested that males and females have concordant carotenoid pigment profiles across all species (MCMCglmm model, female:male ratio = 0.95). Male, but not female, feathers have elaborate microstructures which amplify color appearance. Oblong, expanded feather barbs in males enhance color saturation (for the same amount of pigment) by increasing the transmission of optical power through the feather. Dihedral barbules (vertically-angled, strap-shaped barbules) in males reduce total reflectance to generate "super black" and "velvet red" plumage. Melanin in females explains some, but not all, of the male-female plumage differences. Our results suggest that a widely cited index of honesty, carotenoid pigments, cannot fully explain male appearance. We propose that males are selected to evolve amplifiers-in this case, microstructures that enhance appearance-that are not necessarily themselves linked to quality.

Embryo Selection and Mate Choice: Can 'Honest Signals' Be Trusted?

When a measure becomes a target, it often ceases to be a good measure - an effect familiar from the declining usefulness of standardized testing in schools. This economic principle also applies to mate choice and, perhaps surprisingly, pregnancy. Just as females screen potential mates under many metrics, human mothers unconsciously screen embryos for quality. 'Examinees' are under intense selection to improve test performance by exaggerating formerly 'honest' signals of quality. Examiners must change their screening criteria to maintain useful information (but cannot abandon old criteria unilaterally). By the resulting 'proxy treadmill', new honest indicators arise while old degraded indicators linger, resulting in trait elaboration and exaggeration. Hormone signals during pregnancy show extreme evolutionary escalation (akin to elaborate mating displays).

Delayed gratification in New Caledonian crows and young children: influence of reward type and visibility.

Self-control underlies cognitive abilities such as decision making and future planning. Delay of gratification is a measure of self-control and involves obtaining a more valuable outcome in the future by tolerating a delay or investing a greater effort in the present. Contextual issues, such as reward visibility and type, may influence delayed gratification performance, although there has been limited comparative investigation between humans and other animals, particularly non-primate species. Here, we adapted an automated 'rotating tray' paradigm used previously with capuchin monkeys to test for delay of gratification ability that requires little pre-test training, where the subject must forgo an immediate, less preferred reward for a delayed, more preferred one. We tested New Caledonian crows and 3-5-year-old human children. We manipulated reward types to differ in quality or quantity (Experiments 1 and 2) as well as visibility (Experiment 2). In Experiments 1 and 2, both species performed better when the rewards varied in quality as opposed to quantity, though performed above chance in both conditions. In Experiment 1, both crows and children were able to delay gratification when both rewards were visible. In Experiment 2, 5-year-old children outperformed 3- and 4-year olds, though overall children still performed well, while the crows struggled when reward visibility was manipulated, a result which may relate to difficulties in tracking the experimenters' hands during baiting. We discuss these findings in relation to the role of contextual issues on self-control when making species comparisons and investigating the mechanisms of self-control.

Convergent evolution of super black plumage near bright color in 15 bird families.

We examined extremely low-reflectance, velvety black plumage patches in 32 bird species from 15 families and five orders and compared them with 22 closely related control species with normal black plumage. We used scanning electron microscopy to investigate microscopic feather anatomy, and applied spectrophotometry and hyperspectral imaging to measure plumage reflectance. Super black plumages are significantly darker and have more broadband low reflectance than normal black plumages, and they have evolved convergently in 15 avian families. Super black feather barbules quantitatively differ in microstructure from normal black feathers. Microstructural variation is significantly correlated with reflectance: tightly packed, strap-shaped barbules have lower reflectance. We assigned these super black feathers to five heuristic classes of microstructure, each of which has evolved multiple times independently. All classes have minimal exposed horizontal surface area and 3D micrometer-scale cavities greater in width and depth than wavelengths of light. In many species, barbule morphology varied between the super black exposed tip of a feather and its (i) concealed base or (ii) iridescently colored spot. We propose that super black plumages reduce reflectance, and flatten reflectance spectra, through multiple light scattering between the vertically oriented surfaces of microscale cavities, contributing to near-complete absorption of light by melanin. All super black plumage patches identified occur adjacent to brilliant colored patches. Super black plumage lacks all white specular reflections (reference points used to calibrate color perception), thus exaggerating the perceived brightness of nearby colors. We hypothesize that this sensory bias is an unavoidable by-product of color correction in variable light environments.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys.

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.

New Caledonian Crows Behave Optimistically after Using Tools.

Are complex, species-specific behaviors in animals reinforced by material reward alone or do they also induce positive emotions? Many adaptive human behaviors are intrinsically motivated: they not only improve our material outcomes, but improve our affect as well [1-8]. Work to date on animal optimism, as an indicator of positive affect, has generally focused on how animals react to change in their circumstances, such as when their environment is enriched [9-14] or they are manipulated by humans [15-23], rather than whether complex actions improve emotional state. Here, we show that wild New Caledonian crows are optimistic after tool use, a complex, species-specific behavior. We further demonstrate that this finding cannot be explained by the crows needing to put more effort into gaining food. Our findings therefore raise the possibility that intrinsic motivation (enjoyment) may be a fundamental proximate cause in the evolution of tool use and other complex behaviors. VIDEO ABSTRACT.

Structurally assisted super black in colourful peacock spiders.

Male peacock spiders ( Maratus, Salticidae) compete to attract female mates using elaborate, sexually selected displays. They evolved both brilliant colour and velvety black. Here, we use scanning electron microscopy, hyperspectral imaging and finite-difference time-domain optical modelling to investigate the deep black surfaces of peacock spiders. We found that super black regions reflect less than 0.5% of light (for a 30° collection angle) in Maratus speciosus (0.44%) and Maratus karrie (0.35%) owing to microscale structures. Both species evolved unusually high, tightly packed cuticular bumps (microlens arrays), and M. karrie has an additional dense covering of black brush-like scales atop the cuticle. Our optical models show that the radius and height of spider microlenses achieve a balance between (i) decreased surface reflectance and (ii) enhanced melanin absorption (through multiple scattering, diffraction out of the acceptance cone of female eyes and increased path length of light through absorbing melanin pigments). The birds of paradise (Paradiseidae), ecological analogues of peacock spiders, also evolved super black near bright colour patches. Super black locally eliminates white specular highlights, reference points used to calibrate colour perception, making nearby colours appear brighter, even luminous, to vertebrates. We propose that this pre-existing, qualitative sensory experience-'sensory bias'-is also found in spiders, leading to the convergent evolution of super black for mating displays in jumping spiders.

Structural absorption by barbule microstructures of super black bird of paradise feathers.

Many studies have shown how pigments and internal nanostructures generate color in nature. External surface structures can also influence appearance, such as by causing multiple scattering of light (structural absorption) to produce a velvety, super black appearance. Here we show that feathers from five species of birds of paradise (Aves: Paradisaeidae) structurally absorb incident light to produce extremely low-reflectance, super black plumages. Directional reflectance of these feathers (0.05-0.31%) approaches that of man-made ultra-absorbent materials. SEM, nano-CT, and ray-tracing simulations show that super black feathers have titled arrays of highly modified barbules, which cause more multiple scattering, resulting in more structural absorption, than normal black feathers. Super black feathers have an extreme directional reflectance bias and appear darkest when viewed from the distal direction. We hypothesize that structurally absorbing, super black plumage evolved through sensory bias to enhance the perceived brilliance of adjacent color patches during courtship display.