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Structurally Assisted Super Black in Colourful Peacock Spiders

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Structurally Assisted Super Black in Colourful Peacock Spiders Downloaded from orbit.dtu.dk on: Sep 24, 2021 Structurally assisted super black in colourful peacock spiders McCoy, Dakota E.; McCoy, Victoria E.; Mandsberg, Nikolaj Kofoed; Shneidman, Anna V.; Aizenberg, Joanna; Prum, Richard O.; Haig, David Published in: Proceedings of the Royal Society B: Biological Sciences Link to article, DOI: 10.1098/rspb.2019.0589 Publication date: 2019 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): McCoy, D. E., McCoy, V. E., Mandsberg, N. K., Shneidman, A. V., Aizenberg, J., Prum, R. O., & Haig, D. (2019). Structurally assisted super black in colourful peacock spiders. Proceedings of the Royal Society B: Biological Sciences, 286(1902), [20190589]. https://doi.org/10.1098/rspb.2019.0589 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Structurally assisted super black royalsocietypublishing.org/journal/rspb in colourful peacock spiders Dakota E. McCoy1, Victoria E. McCoy2, Nikolaj K. Mandsberg3,4, Anna V. Shneidman4, Joanna Aizenberg4,5,6, Richard O. Prum7 Research and David Haig1 1 Cite this article: McCoy DE, McCoy VE, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA Mandsberg NK, Shneidman AV, Aizenberg J, 2Steinmann-Institut fu¨r Geologie, Mineralogie und Pala¨ontologie, Universita¨t Bonn, Nussallee 8, 53115 Bonn, Prum RO, Haig D. 2019 Structurally assisted Germany super black in colourful peacock spiders. 3Department of Health Technology, Technical University of Denmark, 2800 Kongens Lyngby, Denmark 4John A. Paulson School of Engineering and Applied Sciences, Harvard University, 9 Oxford Street, Cambridge, Proc. R. Soc. B 286: 20190589. MA 02138, USA http://dx.doi.org/10.1098/rspb.2019.0589 5Department of Chemistry and Chemical Biology, Harvard University, 12 Oxford Street, Cambridge, MA, USA 6Kavli Institute for Bionano Science and Technology, Harvard University, 29 Oxford Street, Cambridge, MA, USA 7Department of Ecology and Evolutionary Biology, and Peabody Museum of Natural History, Yale University, New Haven, CT 06511, USA Received: 12 March 2019 DEM, 0000-0001-8383-8084; VEM, 0000-0002-5655-0381; NKM, 0000-0003-3285-3887; Accepted: 23 April 2019 AVS, 0000-0001-6064-5378; JA, 0000-0002-2343-8705; DH, 0000-0001-7377-1605 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 Subject Category: imaging and finite-difference time-domain optical modelling to investigate Evolution the deep black surfaces of peacock spiders. We found that super black regions reflect less than 0.5% of light (for a 308 collection angle) in Maratus speciosus Subject Areas: (0.44%) and Maratus karrie (0.35%) owing to microscale structures. Both species evolution, biomaterials evolved unusually high, tightly packed cuticular bumps (microlens arrays), and M. karrie has an additional dense covering of black brush-like scales atop Keywords: the cuticle. Our optical models show that the radius and height of spider micro- lenses achieve a balance between (i) decreased surface reflectance and (ii) microlens arrays, structural colour, peacock enhanced melanin absorption (through multiple scattering, diffraction out of spiders, sexual selection 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 Author for correspondence: patches. Super black locally eliminates white specular highlights, reference points used to calibrate colour perception, making nearby colours appear Dakota E. McCoy brighter, even luminous, tovertebrates. We propose that this pre-existing, quali- e-mail: [email protected] tative sensory experience—‘sensory bias’—is also found in spiders, leading to the convergent evolution of super black for mating displays in jumping spiders. 1. Background Colour plays a number of roles in inter- or intra-specific visual signalling, includ- ing camouflage, mimicry, warning coloration and social signalling [1]. Some of the most elaborate colour displays have evolved because of sexual selection by mate choice [2–5], exemplified by the peacock spiders (Maratus, Salticidae [6]), which are subject to unusually intense sexual selection [7]. Among males, com- petition to be preferred by females and secure mating opportunities has produced innovative visual traits at multiple size scales [6,8–11]. Investigating these stimulating visual displays can (i) reveal novel colour-producing mechan- isms [10,12], (ii) inform our understanding of animals’ visual ecology and Electronic supplementary material is available sensory experiences [8,13], and (iii) guide the design of human-made devices for colour production and other forms of light manipulation [12]. online at https://dx.doi.org/10.6084/m9. figshare.c.4486193. & 2019 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. 2 (a) (c) (d) royalsocietypublishing.org/journal/rspb (e) ( f ) (b) Proc. R. Soc. B (g) (h) 286 : 20190589 Figure 1. Deep black patches alongside brilliant colours in peacock spiders (a–g), and a closely related shiny black spider (h). (a) Maratus speciosus,(b) Maratus karrie,(c) Maratus nigromaculatus,(d) Maratus robinsoni,(e) Maratus hortorum,(f ) Maratus avibus,(g) Maratus chrysomelas and (h) Cylistella sp. Scale bars are all 1 mm; for (a–g), they are estimated based on species-typical size. Scale bars are taken from: (a,b) specimen measurements herein, (c) [20,21], (d) [20], (e) [22], (f ) [23], (g) [24] and (h) Facundo Martı´n Labarque. Pictures are courtesy of (a–g)Ju¨rgen Otto and (h) Facundo Martı´n Labarque and may not be reproduced. The highly visual, polygynous jumping spiders (Saltici- among barbule microstructures which greatly enhances the dae) have elaborate displays of bright colours and efficiency of melanin absorption [31]. More generally, super behaviours [6,14]. Particularly, male jumping spiders of the black is defined as structural or structurally assisted absorption genus Maratus, known as peacock spiders, have splendidly with significantly reduced specular reflectance compared coloured abdomens which they erect and wave side-to-side to that of a flat (unstructured) surface of the same material during mating displays to females [6,8,9]. Structural colours [31–33]. In nature, anti-reflection (whether in combination in peacock spiders are produced by plate-like blue scales with pigmentary absorption or not) has evolved in moth (modified setae) with a dual thin film structure [10] or rain- eyes to reduce glare [34], in transparent aquatic animals to bow scales with two-dimensional diffraction gratings atop a evade detection [35], in glasswing butterflies to avoid avian convex three-dimensional microstructure [12]. Brush-like predators [36], in velvet black spots on a viper to merge into scales produce cream, yellow or red colours through pig- shadows on the forest floor [37] and more—and frequently ments in combination with structural effects [10,14]. Other has inspired anti-reflective engineered materials (e.g. [38]). brush-like black scales contain melanins [12,15]. There is Super black coloration is extremely low reflectance (e.g. less strong mate choice by female peacock spiders for strikingly than 0.5% directional reflectance in birds of paradise), bright and bold colour patterns; jumping spiders have approaching the darkest human-made materials available acute colour vision [16,17] and colourful male ornaments [39–41]; this raises the question of why such an intricate, are the direct targets of female choice [7,18,19]. Furthermore, extreme trait evolved. In birds of paradise, super black may female peacock spiders are extremely choosy and usually have evolved through sensory bias [31], whereby a trait stimu- mate only once [6]. Therefore, males are under powerful lates pre-existing sensory/cognitive biases and preferences in selective pressure to fulfil female preferences. females [4,42,43]. Specifically, in a variety of vertebrates, Intriguingly, males of many species of peacock spiders super black surfaces impede natural mechanisms of colour cor- have dark, velvety black patches adjacent to bright colour rection by removing white specular highlights that are used as patches (figure 1). This is reminiscent of the super black white-balancing reference points, causing nearby colours to plumage near bright colours in the birds of paradise (Paradi- appear brighter—even
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