The ocular skeleton through the eye of evo-devo

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<ul><li><p>The Ocular Skeleton Throughthe Eye of Evo-DevoTAMARA ANNE FRANZ-ODENDAAL</p><p>Biology Department, Mount Saint Vincent University, Halifax, Nova Scotia, Canada</p><p>An evolutionary developmental (evo-devo) approach to understanding the evolution, homology, anddevelopment of structures has proved important for unraveling complex integrated skeletal systemsthrough the use of modules, or modularity. An ocular skeleton, which consists of cartilage andsometimes bone, is present in many vertebrates; however, the origin of these two componentsremains elusive. Using both paleontological and developmental data, I propose that the vertebrateocular skeleton is neural crest derived and that a single cranial neural crest module divided early invertebrate evolution, possibly during the Ordovician, to give rise to an endoskeletal component and anexoskeletal component within the eye. These two components subsequently became uncoupled withrespect to timing, placement within the sclera and inductive epithelia, enabling them to evolveindependently and to diversify. In some extant groups, these two modules have become reassociatedwith one another. Furthermore, the data suggest that the endoskeletal component of the ocularskeleton was likely established and therefore evolved before the exoskeletal component. This studyprovides important insights into the evolution of the ocular skeleton, a region with a long evolutionaryhistory among vertebrates. J. Exp. Zool. (Mol. Dev. Evol.) 316:393401, 2011. &amp; 2011 Wiley-Liss, Inc.</p><p>How to cite this article: Franz-Odendaal TA. 2011. The ocular skeleton through the eye ofevo-devo. J. Exp. Zool. (Mol. Dev. Evol.) 316:393401.</p><p>The ocular skeleton of vertebrates is well known among</p><p>paleontologists as enigmatic structures within the eye whose</p><p>function, origin, and homology are not well understood. The</p><p>ocular skeleton can consist of bone and/or cartilage. Two general</p><p>morphologies are recognized: (i) a multi-component ring of</p><p>several scleral ossicles with a separate scleral cartilage cup</p><p>supporting the eyeball (e.g. in reptiles) (Fig. 1); or (ii) two scleral</p><p>ossicles joined by scleral cartilage (e.g. in advanced teleosts)</p><p>(Fig. 2). Importantly, the relationship between the scleral ossicles</p><p>and the scleral cartilage is different in each of these morphologies</p><p>(Franz-Odendaal and Hall, 2006a).</p><p>In 1929, Dr. Tilly Edinger published the first comparative</p><p>study on the scleral ossicles of both fossil and modern vertebrates</p><p>in an attempt to try and resolve some of these complexities</p><p>(Edinger, 29). More recently, Franz-Odendaal and Hall (2006a)</p><p>provided an updated assessment of the presence and absence of</p><p>scleral ossicles and scleral cartilage within the eyes of extant</p><p>vertebrates. From this analysis, we concluded that the ocular</p><p>skeleton(s) of extant teleosts and reptiles differs morphologically</p><p>and in their mode of ossification. Furthermore, presuming a</p><p>common ancestral ocular skeleton, we hypothesized that the</p><p>scleral ossicles of extant reptiles and extant teleosts cannot be</p><p>assumed to be homologous to one another (Franz-Odendaal and</p><p>Hall, 2006a).</p><p>The evolution of ocular skeleton is particularly complex to</p><p>resolve because at various time points (and/or in various</p><p>lineages) during vertebrate evolution one or both components</p><p>may be absent. There is also a large variability in the morphology</p><p>of the ocular skeleton specifically with respect to its overall</p><p>structure (a capsule or a ring of plates/ossicles), and with respect</p><p>to the individual ossicles within the sclerotic ring, which can be</p><p>variable in shape, size, and number, both among different</p><p>vertebrate groups and within taxa (Franz-Odendaal and Hall,</p><p>2006a; Franz-Odendaal, 2011) (Figs. 1 and 2). Together, this</p><p>variability in the ocular skeletal morphology significantly</p><p>complicates any attempt at an evolutionary assessment. Here,</p><p>I attempt to resolve the evolutionary history of the ocular</p><p>skeleton by reassessing its morphology in the jawless vertebrates.</p><p>Published online 19 April 2011 in Wiley Online Library (wileyonline</p><p> DOI: 10.1002/jez.b.21415</p><p>Received 25 October 2010; Revised 22 February 2011; Accepted 24 March</p><p>2011</p><p>Grant Sponsor: Natural Sciences and Engineering Research Council, Canada;</p><p>Grant number: DG ] 328376.Correspondence to: Tamara Anne Franz-Odendaal, Biology Department,</p><p>Mount Saint Vincent University, Halifax, Nova Scotia, Canada B3M 2J6.</p><p>E-mail:</p><p>ABSTRACT</p><p>J. Exp. Zool.(Mol. Dev. Evol.)316:393401, 2011</p><p>&amp; 2011 WILEY-LISS, INC.</p><p>PERSPECTIVE AND HYPOTHESIS</p></li><li><p>Figure 1. Schematics showing some of the variation in scleral ossicle shape and size, the amount of cartilage support and the size of the eye</p><p>aperture within Reptilia. (A) The European green lizard Lacerta viridis, (B) the legless lizard, Anguis fragilis, (C) the gecko Gehyra mutilata, and</p><p>the chicken Gallus gallus. The cartilage support in D is very large compared with the very reduced cartilage element in A and C (a cup vs. a</p><p>disk). Shaded regions show scleral cartilage; unshaded regions indicate scleral ossicles.</p><p>Figure 2. Schematic of teleost scleral ossicles and scleral cartilage, lateral view of the eye with the ossicles situated anterior and posteriorly</p><p>within the eye. (A) Two large ossicles as seen in salmon, Salmo salar, for example; (B) the two small ossicles of the pike, Esox; and (C) the</p><p>complete scleral cartilage ring of the American eel, Anguilla rostrata. For phylogentic distribution, see Franz-Odendaal et al. (2008b). Shaded</p><p>regions show scleral cartilage; unshaded regions indicate scleral ossicles.</p><p>FRANZ-ODENDAAL394</p><p>J. Exp. Zool. (Mol. Dev. Evol.)</p></li><li><p>I then apply the evolutionary developmental (evo-devo) concept</p><p>of modularity (described below) to this data set and discuss the</p><p>evolutionary origin of these elements.</p><p>Endoskeleton or Exoskeleton?</p><p>Within the paleontological field, ossifications within the eye have</p><p>been reported as one of two morphologies; either as scleral</p><p>ossicles (a series of dermal bones) and/or as an ossified</p><p>endoskeletal scleral capsule within the eye (e.g. in Donoghue</p><p>et al., 2000). This is an important distinction. Although many</p><p>agree that the presence of scleral ossicles is a unifying character</p><p>of gnathostomes and Osteostraci (Maisey, 86; Donoghue et al.,</p><p>2000), the presence of an additional endoskeletal scleral capsule</p><p>is less certain. Several authors, for example, code Osteostraci as</p><p>having both scleral ossicles and an ossified endoskeletal scleral</p><p>capsule encapsulating the eyeball (Donoghue et al., 2000; Gess</p><p>et al., 2006). Others do not make this distinction (Zhu et al., 99).</p><p>I have reassessed the ocular skeleton at major nodes of</p><p>vertebrate evolution based on the published literature. However,</p><p>before discussing these data, we should examine the use of the</p><p>term endoskeletal vs. exoskeletal. Most of the vertebrate skeleton</p><p>of extant animals consists of bone and cartilage, is internal and is</p><p>considered endoskeletal. The exoskeleton arose as denticles in</p><p>association with ectoderm, and consists of bone and dentine with</p><p>no cartilage components. During vertebrate evolution, the</p><p>exoskeleton has been greatly reduced. The endoskeletal cartilage</p><p>on the other hand either persisted as permanent cartilage, or as</p><p>mineralized cartilage (as in sharks) or was replaced by bone (via</p><p>endochondral ossification; Smith and Hall, 90). With respect to</p><p>germ layer origins, the endoskeleton is mesodermal or neural</p><p>crest derived, whereas the exoskeleton is always neural crest</p><p>derived. The neural crest cells migrate out of the neural folds</p><p>during neural tube formation and are considered derivatives of</p><p>the neural ectoderm.</p><p>Regarding the ocular skeleton, the scleral ossicles of extant</p><p>reptiles are induced by ectoderm and do not preform in cartilage,</p><p>and therefore should be considered exoskeletal; the scleral</p><p>cartilage cup situated more posteriorly in the eye, however, is a</p><p>permanent or persistent cartilage and should be considered</p><p>endoskeletal. In advanced teleosts, in which two scleral ossicles</p><p>are joined by scleral cartilage, the situation is different. Here, the</p><p>scleral ossicles develop via a form of endochondral ossification</p><p>from a cartilage template (Franz-Odendaal et al., 2007). Both</p><p>components in extant teleosts should therefore be considered</p><p>endoskeletal. In summary, only the scleral ossicles of extant</p><p>reptiles are exoskeletal, whereas all the other components of the</p><p>ocular skeleton of extant vertebrates are endoskeletal.</p><p>A Phylogenetic Assessment</p><p>In addition to the differences in the terminology used to describe</p><p>the ocular skeleton, this region of the skeleton has been character</p><p>coded in inconsistent ways with respect to the number of</p><p>elements. Zhu et al. (99) coded the number of scleral plates/</p><p>ossicles: 0 for four or less plates; 1 for greater than four plates. In</p><p>contrast, Donoghue et al. (2000) coded the ocular skeleton in two</p><p>characters. One character for scleral ossicles, regardless of</p><p>number of elements: 0 if the ossicles were absent; 1 if they were</p><p>present. The second character was the ossified endoskeletal</p><p>sclera: 0 if absent; 1 if present. Other paleontologists are less</p><p>clear, for example, figures given in Luksevics and Vin (2001),</p><p>describe the ocular skeleton of Asterolepis (a placoderm) as a</p><p>scleral capsule yet the figure shows a ring and is labeled as</p><p>Sclr for sclerotic ring.</p><p>A re-coding of the ocular skeleton at major nodes of</p><p>vertebrate evolution based on the published literature is needed</p><p>and should help to unravel this data; ultimately it should help us</p><p>to understand the evolution of the ocular skeleton (Fig. 3). We</p><p>have previously hypothesized about the homology of the</p><p>components of the ocular skeleton based on data from extant</p><p>actinopterygians and extant sarcopterygians. The focus in this</p><p>manuscript is to go further back in vertebrate history and to</p><p>examine the ocular skeleton of jawless vertebrates. To do this, the</p><p>ocular skeleton as a single entity was assessed as present or</p><p>absent in each group, regardless of the number of elements, the</p><p>type of ossification, the shape (capsule vs. ring), or skeletal type</p><p>(endoskeleton vs. exoskeleton). Second, the (endoskeletal vs.</p><p>exoskeletal) components were coded, regardless of their mor-</p><p>phology. These data are presented and summarized in Figure 3.</p><p>The ocular skeleton is present in extant gnathostomes</p><p>(Sarcopterygii, Actinopterygii, and Chondrichthyes) as well as</p><p>in basal gnathostomes such as placoderms (Table 1, Fig. 3). Most</p><p>placoderms have scleral ossicles and some have dermal</p><p>ornamentation on these bones (Burrow et al., 2005). However</p><p>in one placoderm (Jagorina) the ocular skeleton has been</p><p>described as an ossified capsule fused to a sclerotic ring of bones</p><p>(Stensio, 50; Luksevics and Vin, 2001); that is both components</p><p>of the ocular skeleton are present. In acanthodians, a sclerotic</p><p>ring is described in some forms (Acanthodes, Homalacanthus)</p><p>while others (Climatius, Ptomacanthus, Euthacanthus, Brachya-</p><p>canthus, Cassidiceps) possess circumorbital plates (Gagnier, 96).</p><p>Watson (37) however, considered the ring in all these</p><p>acanthodians as circumorbital plates. Friedman and Brazeau</p><p>(2010) note that no acanthodian has both a sclerotic ring and</p><p>circumorbital plates, begging the question of their homology. To</p><p>unravel this status, these groups should be re-examined (see</p><p>recent work by Burrow et al., 2011); however, this is not the focus</p><p>of the current review. To summarize, the fossil record of jawed</p><p>vertebrates provides evidence for an ocular skeleton in all groups</p><p>(placoderms, acanthodians, Osteichthyes, and Chondichthyes).</p><p>Within jawless vertebrates, no ocular skeleton is known from</p><p>Eriptychius; however, this fossil is known from fragmentary</p><p>elements only. An ocular skeleton is described in Osteostraci as</p><p>an endoskeletal capsule with scleral ossicles (Edinger, 29; Walls,</p><p>63; Donoghue et al., 2000; Gess et al., 2006). The ocular skeleton</p><p>SCLERAL OSSICLE EVOLUTION 395</p><p>J. Exp. Zool. (Mol. Dev. Evol.)</p></li><li><p>is absent in Galeaspids, Heterostraci, Anaspida, Jamoytius,</p><p>Euphanerops, and Loganellia (Edinger, 29; Gess et al., 2006).</p><p>Interestingly, there is evidence for an ocular skeleton in the</p><p>Ordovician before the evolution of the above groups; both</p><p>Astraspis and Arandaspida have an ocular skeleton (Gess et al.,</p><p>2006). Astraspis has an ossified endoskeletal capsule without</p><p>scleral ossicles, whereas Arandaspida has both an ossified</p><p>endoskeletal capsule and (exoskeletal) scleral ossicles. The</p><p>identification of both scleral ossicles and an endoskeletal capsule</p><p>within the eye of Arandaspida is based on a single observation by</p><p>Gagnier (93), but has been confirmed by Donoghue et al. (2000).</p><p>Groups without an ocular skeleton may have had, and most likely</p><p>had, unmineralised connective tissue within the sclera (e.g. as</p><p>described in conodonts and as is evident in some extant</p><p>vertebrates such as placental mammals; Walls, 63).</p><p>This known evolutionary history, places the origin for the</p><p>ocular skeleton before the evolution of Astraspis and Arandas-</p><p>pida (dating to Ordovician 480440 million years ago; Fig. 3).</p><p>Hence, both exoskeletal and endoskeletal components had</p><p>evolved at this time. Given that the exoskeletal component is</p><p>never found without an endoskeletal component and given that</p><p>Astraspis possesses the endoskeletal component alone, the most</p><p>likely hypothesis is that the endoskeletal component (the</p><p>cartilage-based component) was established first (i.e. before the</p><p>exoskeletal component). Interestingly, 480 million years ago is</p><p>shortly after the proposed origin of bone and dentine, cartilage</p><p>having arose earlier (between 540 and 525 million years ago)</p><p>(Donoghue et al., 2008; Fig. 3).</p><p>In terms of cellular origins, the exoskeleton is neural crest</p><p>derived, whereas the endoskeleton has a mixed origin of neural</p><p>crest and mesoderm. It is also well known that the entire avian</p><p>ocular skeleton is neural crest derived (Couly et al., 93; Franz-</p><p>Odendaal and Vickaryous, 2006). Other data using a sox10-green</p><p>fluorescent protein-tagged transgenic zebrafish line indicates that</p><p>the ocular skeleton of teleosts is also neural crest derived</p><p>(unpublished observation). Regarding fossil specimens, Donoghue</p><p>and colleagues have also shown that the neural crest evolved in the</p><p>Cambrian, and that the molecular tools required to specify the</p><p>neural crest were also present in early vertebrates (hagfishes and</p><p>lampreys) (Donoghue et al., 2000, 2008). In summary, the neural</p><p>crest was well-established at the time of the origin of the ocular</p><p>skeleton and the opportunity to pattern this cell population was</p><p>presumably also present. Indeed, the tissue responsible for inducing</p><p>the scleral cartilage, the retinal pigmented epithelium, was present</p><p>Figure 3. Phylogenetic distribution of the presence and absence of the ocular skeleton within vertebrates. The status of the ocular skeleton</p><p>regardless of origin, morphology, or development is denoted by the terms, present, absent, or unknown. This is followed by a coding for the</p><p>type of ocular skeleton. The first valu...</p></li></ul>