Towards a Better Understanding of the Origins of Microlens Arrays in Mesozoic Ophiuroids and Asteroids
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Towards a Better Understanding of the Origins of Microlens Arrays in Mesozoic Ophiuroids and Asteroids Przemysław Gorzelak, Imran A. Rahman, Samuel Zamora, Arkadiusz Gąsiński, Jerzy Trzciński, Tomasz Brachaniec & Mariusz A. Salamon Evolutionary Biology Evolutionary Biology ISSN 0071-3260 Evol Biol DOI 10.1007/s11692-017-9411-1 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media New York. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Evol Biol DOI 10.1007/s11692-017-9411-1 RESEARCH ARTICLE Towards a Better Understanding of the Origins of Microlens Arrays in Mesozoic Ophiuroids and Asteroids Przemysław Gorzelak1 · Imran A. Rahman2 · Samuel Zamora3,4 · Arkadiusz Gąsiński5 · Jerzy Trzciński6 · Tomasz Brachaniec7 · Mariusz A. Salamon8 Received: 15 September 2016 / Accepted: 10 February 2017 © Springer Science+Business Media New York 2017 Abstract Echinoderms are characterized by a calcite detail. The results indicate that, similar to Recent light-sen- endoskeleton with a unique microstructure, which is opti- sitive ophiuroids, putative microlenses in Cretaceous ophi- mized for multiple functions. For instance, some light- uroids and asteroids exhibit a shape and crystal orientation sensitive ophiuroids (Ophiuroidea) and asteroids (Aster- that would have minimized spherical aberration and bire- oidea) possess skeletal plates with multi-lens arrays that are fringence. We suggest that these lens-like microstructures thought to act as photosensory organs. The origins of these evolved by secondary deposition of calcite on pre-existing lens-like microstructures have long been unclear. It was porous tubercles that were already present in ancestral recently proposed that the complex photosensory systems Jurassic forms. in certain modern ophiuroids and asteroids could be traced back to at least the Late Cretaceous (ca. 79 Ma). Here, we Keywords Echinoderms · Photosensitivity · Cretaceous · document similar structures in ophiuroids and asteroids Microlenses · Calcite · Tomography from the Early Cretaceous of Poland (ca. 136 Ma) that are approximately 57 million years older than the oldest aste- rozoans with lens-like microstructures described thus far. Introduction We use scanning electron microscopy, synchrotron tomog- raphy, and electron backscatter diffraction combined with Echinoderms exploit their calcite endoskeleton for a vari- focused ion beam microscopy to describe the morphol- ety of functions, including support, movement, protec- ogy and crystallography of these structures in exceptional tion, food gathering, and ion storage (Smith 1990). This multipurpose tissue can be modelled into different shapes through the use of an amorphous calcium carbonate pre- Electronic supplementary material The online version of this article (doi:10.1007/s11692-017-9411-1) contains supplementary cursor and the involvement of organic molecules during material, which is available to authorized users. 5 * Przemysław Gorzelak Institute of Geochemistry, Mineralogy and Petrology, Faculty [email protected] of Geology, University of Warsaw, Żwirki i Wigury 93, 02-089 Warsaw, Poland * Mariusz A. Salamon 6 [email protected] Institute of Hydrogeology and Engineering Geology, Faculty of Geology, University of Warsaw, Żwirki i Wigury 93, 1 Institute of Paleobiology, Polish Academy of Sciences, 02-089 Warsaw, Poland Twarda 51/55, 00-818 Warsaw, Poland 7 Department of Geochemistry, Mineralogy and Petrography, 2 Oxford University Museum of Natural History, Parks Road, Faculty of Earth Sciences, University of Silesia, Będzińska Oxford OX1 3PW, UK 60, 41-200 Sosnowiec, Poland 8 3 Instituto Geológico y Minero de España (IGME), C/Manuel Department of Palaeontology and Stratigraphy, Faculty Lasala, 44, 9ºB, 50006 Zaragoza, Spain of Earth Sciences, University of Silesia, Będzińska 60, 41-200 Sosnowiec, Poland 4 Unidad Asociada en Ciencias de la Tierra, Universidad de Zaragoza-IGME, Zaragoza, Spain Vol.:(0123456789)1 3 Author's personal copy Evol Biol the biomineralization process (e.g. Politi et al. 2004; Kil- Campanian (ca. 79 Ma) (Gorzelak et al. 2014). Although lian and Wilt 2008). The role of the echinoderm skeleton in external faces in fossil asterozoans are commonly covered vision was suggested long ago (Raup 1966), but it is only by various types of granular ornamentation, sometimes recently that scientists have begun to examine this phenom- referred to as tubercles or pustules (e.g. Blake et al. 2000; enon more closely. For instance, it has been shown that Villier et al. 2004), in-depth microstructural investigations some sea urchins use their skeleton as a shielding device for and functional interpretations of these structures are largely photoreceptor cells, forming numerous compound eye units lacking. In this paper, we use state-of-the-art imaging tech- (Ullrich-Lüter et al. 2011). Another, strikingly different niques to describe the morphology of isolated plates from example of using the skeleton as a part of the photorecep- the arms of select Mesozoic ophiuroids and asteroids, and tive system is reported for the light-sensitive ophiocomid compare these to modern specimens with lens-like micro- ophiuroid Ophiocoma wendtii (Hendler and Byrne 1987). structures. The results shed light on the origins and devel- This species changes colour from uniformly dark brown opment of microlens arrays in asterozoans. during the day to grey and black banded at night when it is most active (Hendler 1984). This change is not connected with camouflage, but is related to their sensitivity to light Materials and Methods (Hendler 2004). Indeed, it has been shown that this species possesses calcitic microlens arrays (Figs. 1a–c, 2a, b), sur- Isolated asterozoan plates with lens-like microstructures rounded by pigment-filled chromatophores, which are able were collected by one of us (MAS) during the course of to focus light onto presumably light-sensitive nerve bundles field work on Cretaceous crinoids (Salamon 2009). The (Aizenberg et al. 2001). These microlenses are micron- material came from late Valanginian (ca. 136 Ma) silts scale in size, lightweight, mechanically strong, aberration- intercalated with clayey sands, which are exposed in an free, and birefringence-free, all properties that may be abandoned brick-pit in Wąwał near Tomaszów Mazowiecki applicable to materials science (Zhang 2003; Aizenberg (central Poland, 51°29′50ʺN 20°3′05ʺE, see Kaim 2001). and Hendler 2004). Such lens-like microstructures are also For comparative purposes, we also surveyed mostly iso- present in other light-sensitive ophiocomid species, but do lated plates (>2000 elements in total) of shallow-water not occur in light-insensitive species (Hendler and Byrne ophiuroids and asteroids (mainly belonging to the families 1987). Interestingly, photosensitive proteins (both rhab- Ophiuridae, Goniasteridae, Astropectinidae and Bentho- domeric and ciliary opsins) have been recently identified pectinidae) from the Triassic, Jurassic and Cretaceous of in the arms of the ophiocomid Ophiopsila aranea, which Poland, Lithuania and Czech Rep., which are housed in the possesses similar lens-like microstructures (Delroisse et al. collections of the Department of Earth Sciences, Labora- 2016). This species exhibits a high sensitivity to green tory of Palaeontology and Biostratigraphy, University of wavelengths of light, indicating a directional phototaxis Silesia (GIUS), Sosnowiec, Poland (Electronic Supplemen- likely enhanced by the microlenses (Delroisse et al. 2016). tary Material; for detailed description of sampling sites see Comparable, though not homologous, structures are also Głuchowski 1987; Salamon 2007, 2008, 2009; Salamon present in some shallow-water asteroids (e.g. goniasterids and Zatoń 2007; Villier 2008; Zatoń et al. 2008a, b; Gor- and archasterids) that live within the photic zone (e.g. Mah zelak and Salamon 2009; Salamon and Gorzelak 2010a, b; 2005; Vinogradova et al. 2016). Although focusing light Hess et al. 2011; Salamon et al. 2012). through microlens arrays has yet to be confirmed in these Plates of a specimen of the Recent photosensitive ophi- taxa, their morphology is strikingly similar to the micro- uroid O. wendtii from southeastern Florida, which displays lenses of ophiocomid ophiuroids, and they are thus con- lens-like microstructures, were also investigated. Soft tis- sidered to be involved in photoreception (e.g. Döderlein sues in this ophiuroid were removed by soaking the speci- 1898; Hendler and Byrne 1987; Dubois and Hayt 1990; men in a 5% sodium hypochlorite solution for 2 h at room Mah 2005; Vinogradova et al. 2016). Notably, in the case temperature. of the asteroid Iconaster, it has recently been shown that High-resolution observations on carbon-coated plates the microlenses are largely absent in deep-water sister and of Recent and fossil specimens were performed with a outgroup taxa,