The ocular skeleton through the eye of evo-devo

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  • The Ocular Skeleton Throughthe Eye of Evo-DevoTAMARA ANNE FRANZ-ODENDAAL

    Biology Department, Mount Saint Vincent University, Halifax, Nova Scotia, Canada

    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. & 2011 Wiley-Liss, Inc.

    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.

    The ocular skeleton of vertebrates is well known among

    paleontologists as enigmatic structures within the eye whose

    function, origin, and homology are not well understood. The

    ocular skeleton can consist of bone and/or cartilage. Two general

    morphologies are recognized: (i) a multi-component ring of

    several scleral ossicles with a separate scleral cartilage cup

    supporting the eyeball (e.g. in reptiles) (Fig. 1); or (ii) two scleral

    ossicles joined by scleral cartilage (e.g. in advanced teleosts)

    (Fig. 2). Importantly, the relationship between the scleral ossicles

    and the scleral cartilage is different in each of these morphologies

    (Franz-Odendaal and Hall, 2006a).

    In 1929, Dr. Tilly Edinger published the first comparative

    study on the scleral ossicles of both fossil and modern vertebrates

    in an attempt to try and resolve some of these complexities

    (Edinger, 29). More recently, Franz-Odendaal and Hall (2006a)

    provided an updated assessment of the presence and absence of

    scleral ossicles and scleral cartilage within the eyes of extant

    vertebrates. From this analysis, we concluded that the ocular

    skeleton(s) of extant teleosts and reptiles differs morphologically

    and in their mode of ossification. Furthermore, presuming a

    common ancestral ocular skeleton, we hypothesized that the

    scleral ossicles of extant reptiles and extant teleosts cannot be

    assumed to be homologous to one another (Franz-Odendaal and

    Hall, 2006a).

    The evolution of ocular skeleton is particularly complex to

    resolve because at various time points (and/or in various

    lineages) during vertebrate evolution one or both components

    may be absent. There is also a large variability in the morphology

    of the ocular skeleton specifically with respect to its overall

    structure (a capsule or a ring of plates/ossicles), and with respect

    to the individual ossicles within the sclerotic ring, which can be

    variable in shape, size, and number, both among different

    vertebrate groups and within taxa (Franz-Odendaal and Hall,

    2006a; Franz-Odendaal, 2011) (Figs. 1 and 2). Together, this

    variability in the ocular skeletal morphology significantly

    complicates any attempt at an evolutionary assessment. Here,

    I attempt to resolve the evolutionary history of the ocular

    skeleton by reassessing its morphology in the jawless vertebrates.

    Published online 19 April 2011 in Wiley Online Library (wileyonline

    library.com). DOI: 10.1002/jez.b.21415

    Received 25 October 2010; Revised 22 February 2011; Accepted 24 March

    2011

    Grant Sponsor: Natural Sciences and Engineering Research Council, Canada;

    Grant number: DG ] 328376.Correspondence to: Tamara Anne Franz-Odendaal, Biology Department,

    Mount Saint Vincent University, Halifax, Nova Scotia, Canada B3M 2J6.

    E-mail: Tamara.Franz-Odendaal@msvu.ca

    ABSTRACT

    J. Exp. Zool.(Mol. Dev. Evol.)316:393401, 2011

    & 2011 WILEY-LISS, INC.

    PERSPECTIVE AND HYPOTHESIS

  • 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

    aperture within Reptilia. (A) The European green lizard Lacerta viridis, (B) the legless lizard, Anguis fragilis, (C) the gecko Gehyra mutilata, and

    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

    disk). Shaded regions show scleral cartilage; unshaded regions indicate scleral ossicles.

    Figure 2. Schematic of teleost scleral ossicles and scleral cartilage, lateral view of the eye with the ossicles situated anterior and posteriorly

    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

    complete scleral cartilage ring of the American eel, Anguilla rostrata. For phylogentic distribution, see Franz-Odendaal et al. (2008b). Shaded

    regions show scleral cartilage; unshaded regions indicate scleral ossicles.

    FRANZ-ODENDAAL394

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  • I then apply the evolutionary developmental (evo-devo) concept

    of modularity (described below) to this data set and discuss the

    evolutionary origin of these elements.

    Endoskeleton or Exoskeleton?

    Within the paleontological field, ossifications within the eye have

    been reported as one of two morphologies; either as scleral

    ossicles (a series of dermal bones) and/or as an ossified

    endoskeletal scleral capsule within the eye (e.g. in Donoghue

    et al., 2000). This is an important distinction. Although many

    agree that the presence of scleral ossicles is a unifying character

    of gnathostomes and Osteostraci (Maisey, 86; Donoghue et al.,

    2000), the presence of an additional endoskeletal scleral capsule

    is less certain. Several authors, for example, code Osteostraci as

    having both scleral ossicles and an ossified endoskeletal scleral

    capsule encapsulating the eyeball (Donoghue et al., 2000; Gess

    et al., 2006). Others do not make this distinction (Zhu et al., 99).

    I have reassessed the ocular skeleton at major nodes of

    vertebrate evolution based on the published literature. However,

    before discussing these data, we should examine the use of the

    term endoskeletal vs. exoskeletal. Most of the vertebrate skeleton

    of extant animals consists of bone and cartilage, is internal and is

    considered endoskeletal. The exoskeleton arose as denticles in

    association with ectoderm, and consists of bone and dentine with

    no cartilage components. During vertebrate evolution, the

    exoskeleton has been greatly reduced. The endoskeletal cartilage

    on the other hand either persisted as permanent cartilage, or as

    mineralized cartilage (as in sharks) or was replaced by bone (via

    endochondral ossification; Smith and Hall, 90). With respect to

    germ layer origins, the endoskeleton is mesodermal or neural

    crest derived, whereas the exoskeleton is always neural crest

    derived. The neural crest cells migrate out of the neural folds

    during neural tube formation and are considered derivatives of

    the neural ectoderm.

    Regarding the ocular skeleton, the scleral ossicles of extant

    reptiles are induced by ectoderm and do not preform in cartilage,

    and therefore should be considered exoskeletal; the scleral

    cartilage cup situated more posteriorly in the eye, however, is a

    permanent or persistent cartilage and should be considered

    endoskeletal. In advanced teleosts, in which two scleral ossicles

    are joined by scleral cartilage, the situation is different. Here, the

    scleral ossicles develop via a form of endochondral ossification

    from a cartilage template (Franz-Odendaal et al., 2007). Both

    components in extant teleosts should therefore be considered

    endoskeletal. In summary, only the scleral ossicles of extant

    reptiles are exoskeletal, whereas all the other components of the

    ocular skeleton of extant vertebrates are endoskeletal.

    A Phylogenetic Assessment

    In addition to the differences in the terminology used to describe

    the ocular skeleton, this region of the skeleton has been character

    coded in inconsistent ways with respect to the number of

    elements. Zhu et al. (99) coded the number of scleral plates/

    ossicles: 0 for four or less plates; 1 for greater than four plates. In

    contrast, Donoghue et al. (2000) coded the ocular skeleton in two

    characters. One character for scleral ossicles, regardless of

    number of elements: 0 if the ossicles were absent; 1 if they were

    present. The second character was the ossified endoskeletal

    sclera: 0 if absent; 1 if present. Other paleontologists are less

    clear, for example, figures given in Luksevics and Vin (2001),

    describe the ocular skeleton of Asterolepis (a placoderm) as a

    scleral capsule yet the figure shows a ring and is labeled as

    Sclr for sclerotic ring.

    A re-coding of the ocular skeleton at major nodes of

    vertebrate evolution based on the published literature is needed

    and should help to unravel this data; ultimately it should help us

    to understand the evolution of the ocular skeleton (Fig. 3). We

    have previously hypothesized about the homology of the

    components of the ocular skeleton based on data from extant

    actinopterygians and extant sarcopterygians. The focus in this

    manuscript is to go further back in vertebrate history and to

    examine the ocular skeleton of jawless vertebrates. To do this, the

    ocular skeleton as a single entity was assessed as present or

    absent in each group, regardless of the number of elements, the

    type of ossification, the shape (capsule vs. ring), or skeletal type

    (endoskeleton vs. exoskeleton). Second, the (endoskeletal vs.

    exoskeletal) components were coded, regardless of their mor-

    phology. These data are presented and summarized in Figure 3.

    The ocular skeleton is present in extant gnathostomes

    (Sarcopterygii, Actinopterygii, and Chondrichthyes) as well as

    in basal gnathostomes such as placoderms (Table 1, Fig. 3). Most

    placoderms have scleral ossicles and some have dermal

    ornamentation on these bones (Burrow et al., 2005). However

    in one placoderm (Jagorina) the ocular skeleton has been

    described as an ossified capsule fused to a sclerotic ring of bones

    (Stensio, 50; Luksevics and Vin, 2001); that is both components

    of the ocular skeleton are present. In acanthodians, a sclerotic

    ring is described in some forms (Acanthodes, Homalacanthus)

    while others (Climatius, Ptomacanthus, Euthacanthus, Brachya-

    canthus, Cassidiceps) possess circumorbital plates (Gagnier, 96).

    Watson (37) however, considered the ring in all these

    acanthodians as circumorbital plates. Friedman and Brazeau

    (2010) note that no acanthodian has both a sclerotic ring and

    circumorbital plates, begging the question of their homology. To

    unravel this status, these groups should be re-examined (see

    recent work by Burrow et al., 2011); however, this is not the focus

    of the current review. To summarize, the fossil record of jawed

    vertebrates provides evidence for an ocular skeleton in all groups

    (placoderms, acanthodians, Osteichthyes, and Chondichthyes).

    Within jawless vertebrates, no ocular skeleton is known from

    Eriptychius; however, this fossil is known from fragmentary

    elements only. An ocular skeleton is described in Osteostraci as

    an endoskeletal capsule with scleral ossicles (Edinger, 29; Walls,

    63; Donoghue et al., 2000; Gess et al., 2006). The ocular skeleton

    SCLERAL OSSICLE EVOLUTION 395

    J. Exp. Zool. (Mol. Dev. Evol.)

  • is absent in Galeaspids, Heterostraci, Anaspida, Jamoytius,

    Euphanerops, and Loganellia (Edinger, 29; Gess et al., 2006).

    Interestingly, there is evidence for an ocular skeleton in the

    Ordovician before the evolution of the above groups; both

    Astraspis and Arandaspida have an ocular skeleton (Gess et al.,

    2006). Astraspis has an ossified endoskeletal capsule without

    scleral ossicles, whereas Arandaspida has both an ossified

    endoskeletal capsule and (exoskeletal) scleral ossicles. The

    identification of both scleral ossicles and an endoskeletal capsule

    within the eye of Arandaspida is based on a single observation by

    Gagnier (93), but has been confirmed by Donoghue et al. (2000).

    Groups without an ocular skeleton may have had, and most likely

    had, unmineralised connective tissue within the sclera (e.g. as

    described in conodonts and as is evident in some extant

    vertebrates such as placental mammals; Walls, 63).

    This known evolutionary history, places the origin for the

    ocular skeleton before the evolution of Astraspis and Arandas-

    pida (dating to Ordovician 480440 million years ago; Fig. 3).

    Hence, both exoskeletal and endoskeletal components had

    evolved at this time. Given that the exoskeletal component is

    never found without an endoskeletal component and given that

    Astraspis possesses the endoskeletal component alone, the most

    likely hypothesis is that the endoskeletal component (the

    cartilage-based component) was established first (i.e. before the

    exoskeletal component). Interestingly, 480 million years ago is

    shortly after the proposed origin of bone and dentine, cartilage

    having arose earlier (between 540 and 525 million years ago)

    (Donoghue et al., 2008; Fig. 3).

    In terms of cellular origins, the exoskeleton is neural crest

    derived, whereas the endoskeleton has a mixed origin of neural

    crest and mesoderm. It is also well known that the entire avian

    ocular skeleton is neural crest derived (Couly et al., 93; Franz-

    Odendaal and Vickaryous, 2006). Other data using a sox10-green

    fluorescent protein-tagged transgenic zebrafish line indicates that

    the ocular skeleton of teleosts is also neural crest derived

    (unpublished observation). Regarding fossil specimens, Donoghue

    and colleagues have also shown that the neural crest evolved in the

    Cambrian, and that the molecular tools required to specify the

    neural crest were also present in early vertebrates (hagfishes and

    lampreys) (Donoghue et al., 2000, 2008). In summary, the neural

    crest was well-established at the time of the origin of the ocular

    skeleton and the opportunity to pattern this cell population was

    presumably also present. Indeed, the tissue responsible for inducing

    the scleral cartilage, the retinal pigmented epithelium, was present

    Figure 3. Phylogenetic distribution of the presence and absence of the ocular skeleton within vertebrates. The status of the ocular skeleton

    regardless of origin, morphology, or development is denoted by the terms, present, absent, or unknown. This is followed by a coding for the

    type of ocular skeleton. The first value in parentheses indicates endoskeletal elements; the second value indicates exoskeletal elements.

    15 presence, 05 absence of character. The evolution of neural crest specifiers and effectors from Donoghue et al. (2008) are shown by

    means of a red star. The green circle shows the latest time point when the cranial neural crest module possibly subdivided. Phylogeny

    modified from Donoghue et al. (2000) and Maddison and Schulz (2007).

    FRANZ-ODENDAAL396

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  • in protochordates (Lamb et al., 2007). In addition, based on the

    above evidence from both extant and fossil investigations, it is very

    likely that the vertebrate ocular skeleton is neural crest derived.

    With this conclusion, we are now in a position to ask how the

    cranial neural crest cell population evolved into the ocular

    skeletons we see in extant vertebrates today.

    Table 1. Analysis of the ocular skeleton of fossil specimens within major vertebrate groups, extant information is provided where relevant.

    Order/Family/Genus Ocular skeleton References

    Myxinoidea/Myxinikela None Gess et al. (2006)

    Myxinoidea/Gilpichthys None Donoghue et al. (2000)

    Hyperoartia/Mesomyzon None Gess et al. (2006)

    Hyperoartia/Priscomyzon None Gess et al. (2006)

    Hyperoartia/Mayomyzon None Gess et al. (2006)

    Euconodonta None Gess et al. (2006)

    Pteraspidomorphi/Astraspis Ossified endoskeletal capsule only Gess et al. (2006)

    Pteraspidomorphi/Arandaspida Scleral ossicles present and ossified

    endoskeletal capsule

    Gess et al. (2006)

    Pteraspidomorphi/Heterostraci/Protopterus None Edinger (29)

    Thelodonti/Loganellia None Gess et al. (2006)

    Anaspida/Jamoytius None Gess et al. (2006)

    Anaspida/Euphanerops None Gess et al. (2006)

    Galaespida None Gess et al. (2006)

    Osteotraci/Cephalaspidea Scleral ossicles present Edinger (29)

    Osteotraci/Tremataspis Scleral ossicles present Edinger (29)

    Osteotraci Ossicles and endoskeletal capsule Gess et al. (2006),

    Donoghue et al. (2000),

    Janvier (96)

    Gnathostomes/Actinopterygii/Aspidorhynchus Two bones Edinger (29)

    Gnathostomes/Actinopterygii/Guildayichthyiformes Scleral ossicles present Lund (2000)

    Gnathostomes/Actinopterygii/Palaeonisciformes/Cyranorhis Scleral ossicles present Lund (2000)

    Gnathostomes/Actinopterygii/Palaeonisciformes/Wendyichthys Scleral ossicles present Lund (2000)

    Gnathostomes/Actinopterygii/Palaeonisciformes/Moythomasia Scleral ossicles present Lund (2000)

    Gnathostomes/Actinopterygii/Palaeonisciformes/Cheirolepis Scleral ossicles present Lund (2000), Edinger (29)

    Gnathostomes/Actinopterygii/Semionotiformes/Lepidosteus None de Beer (37)

    Gnathostomes/Actinopterygii/Chondrosteus Scleral ossicles present Edinger (29)

    Gnathostomes/Acanthodii/Acanthodes Scleral ossicles present Moy-Smith and Miles (71)

    Gnathostomes/Sarcopterygii/Osteolepis Scleral ossicles present Edinger (29)

    Gnathostomes/Sarcopterygii/Coelacanthiformes Scleral ossicles present Underwood (70)

    Gnathostomes/Sarcopterygii/Eusthenopteron Scleral ossicles present Zhu et al. (99)

    Gnathostomes/Sarcopterygii/Osteolepis Scleral ossicles present Zhu et al. (99)

    Gnathostomes/Sarcopterygii/Acanthostega Scleral ossicles present Cloutier and Ahlberg (96)

    Gnathostomes/Chondrichthyes (extant forms) Mineralized cup with tesserae

    in some forms

    Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Chondrichthyes/Cladoselache Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Selenosteus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Titanichthys Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Gymnotrachleus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Heintzichthys Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Dunkleosteus Scleral ossicles present Pilgrim and Franz-Odendaal (2009)

    Gnathostomes/Placodermi/Asterolepis Sclerotic capsule Luksevics and Vin (2001)

    Gnathostomes/Placodermi/Jagorina Ossified capsule fused to sclerotic

    ring of ornamental bones

    Stensio (50)

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  • Modules in the Ocular Skeleton

    Applying the concept of modularity to understand the evolu-

    tionary history of complex structures or organisms has proved

    useful in many systems (e.g. limbs: Raff, 96; fins: Mabee

    et al., 2002; cavefish: Franz-Odendaal and Hall, 2006b; skulls:

    Schoch, 2006, etc). A module is a functional, morphological, or

    morphogenetic unit of an organism and is the cellular resource

    for developmental construction and evolutionary variability

    (Atchley and Hall, 91; Raff, 96; Gass and Bolker, 2003; Gass

    and Hall, 2008). Modules are hierarchical and as such can have

    modules nested within them. They are also dynamic and may

    undergo modifications and/or transformations (including dupli-

    cation and divergence). Here, I consider developmental modules,

    which have a unique and intrinsic set of patterning mechanisms

    (Hall, 2005). Similar to the manner in which populations of cells

    can subdivide, so to can modules (Raff, 96). These new modules

    are integrated and able to interact with other modules (Atchley

    and Hall, 91; Gass and Bolker, 2003; Franz-Odendaal and Hall,

    2006b). Recently, Gass and Hall (2008) provided a detailed and

    thoughtful discussion on multicellular modules and concluded

    that each of the four subpopulations of the neural crest cells (i.e.

    cranial, cardiac, trunk, and vagal/sacral) can be considered as

    four separate modules.

    A hypothesis: Following this, one can consider the neural

    crest population that migrates into the eye region (specifically

    into the periocular mesenchyme) as a developmental module. At

    some point during evolution, this population of cells or this

    module subdivided into two modules that could evolve

    independently and at different rates to give rise to the scleral

    cartilage and the scleral ossicle components we see today (Fig. 4).

    One module was positioned posteriorly in the eye and became the

    scleral cartilage (the endoskeletal component) and the other was

    positioned more anteriorly and developed directly into dermal

    bone (the exoskeletal component). Although these two modules

    were uncoupled in the past, they are once again closely

    associated in some extant forms (e.g. in reptiles). The alternative

    hypothesis is that the neural crest population within the eye did

    not subdivide, and that the two components of the ocular

    skeleton we observe today evolved together and dependently.

    Testing the Hypothesis

    Extant sarcopterygians (incl. birds) have two distinct components

    of the ocular skeletonthe scleral cartilage and the scleral ossicles.

    These two components are morphologically, developmentally

    (timing and induction), and perhaps functionally distinct. Both

    the inductive epithelia and the timing of induction of the scleral

    cartilage and the scleral ossicles are distinctly different from one

    another (Franz-Odendaal and Hall, 2006a). In chickens, scleral

    ossicles are induced by the conjunctival epithelium several days

    after the scleral cartilage is induced by the retinal pigment

    epithelium (Coulombre, 65; Newsome, 72; Franz-Odendaal,

    2008a; Thompson et al., 2010). Both of these inductions involve

    epithelial to mesenchymal signaling but their timing and inductive

    tissues are distinct. Therefore, the latter hypothesis that the two

    Figure 4. Schematic showing the cranial neural crest cell (NCC) modules within the eye. (A) Sarcopterygians. A single neural crest

    submodule subdivides. One module evolves to form the scleral cartilage (endoskeletal component) and the other evolves into scleral ossicles

    (i.e. bone via intramembranous ossification) (the exoskeletal component). These modules may be lost over the course of evolution.

    (B) Actinopterygians. The single neural crest module subdivides into two modules. One module is lost, whereas the other evolves into an

    endoskeletal element that may ossify in some teleosts. The ancestral neural crest module is the same module population of cells in A and B,

    and is drawn separately in this schematic for clarity.

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  • modules evolved together and dependently is not supported by

    data from the developmental biology field and can be rejected. The

    alternative hypothesis that the two developmental modules

    evolved independently is discussed below.

    From an evolutionary perspective, one should consider these

    two developmental modules as uncoupled with respect to

    inducing epithelia and timing of induction, despite their close

    association in extant forms today. Because these two modules

    were likely uncoupled for millions of years, the more posterior

    module (that gives rise to the endoskeletal component, the scleral

    cartilage) could have evolved to respond to different epithelia (and

    epithelial signals) and at different times compared with the more

    anterior module (that gives rise to the exoskeletal scleral ossicles

    or the sclerotic ring). This ability to respond to epithelia and to

    then be induced is termed tissue competency and requires a

    distinct change in the activated/inhibited genes. The paleontolo-

    gical data suggest that the subdivision of the neural crest module

    took place before 480440 million years ago (first appearance of

    Astraspis and Arandaspida) and after the Cambrian when the

    neural crest evolved (Donoghue et al., 2000, 2008).

    The hypothesis that the two modules evolved independently is

    further supported by data from extant sarcopterygians in which

    some taxa have secondarily lost one module but maintained the

    other (Walls, 63; Franz-Odendaal and Hall, 2006a) (Fig. 4A). For

    example, snakes only have the endoskeletal module destined to

    form scleral cartilage, and have lost the exoskeletal module destined

    to form scleral ossicles. Other sarcopterygians, such as mammals,

    have lost both modules and still others, such as birds, have retained

    both modules. The mechanism for the complete loss of a module, or

    population of cells, could be via programmed cell death (apoptosis)

    in situations where the cells have become unresponsive to the

    inducing tissues (i.e. lost their competency to respond to inducing

    signals from the epithelium). Changing tissue competency is

    considered to be a major force in the evolution of development

    (Hall, 2000). Alternatively, the neural crest cells may have taken on

    a new (unknown) non-skeletogenic function (neofunctionalisation)

    after leaving the neural tube and before reaching their final

    destination. Most importantly, to date no extant or fossil group has

    retained the exoskeletal component (anterior module) and lost only

    the endoskeletal component (posterior module).

    Furthermore within sarcopterygians, the number of inductive

    events and hence the number of scleral ossicles varies in different

    taxa. Basal sarcopterygians, for example, had many more scleral

    ossicles than living forms therefore the most parsimonious

    explanation is that a reduction in the number of inductive events

    within the anterior module has also taken place over the course

    of evolution (Franz-Odendaal and Hall, 2006a). Epigenetic factors

    that influence condensation sizes and boundaries and hence the

    shape of skeletal elements (Hall and Miyake, 2000; Franz-

    Odendaal, 2011) likely also evolved and changed at this time.

    Consequently, with the ancestral neural crest module subdivid-

    ing early in vertebrate evolution, basal actinopterygians would also

    have had two neural crest-derived modules present within their

    eyes. Teleost scleral ossicles develop via scleral cartilage replace-

    ment (Franz-Odendaal et al., 2007) and these elements are

    endoskeletal (discussed above). Following this logic, the more

    posterior neural crest module persisted within teleosts while the

    anterior module did not evolve further and was probably lost

    before teleost evolution (via apoptosis or neofunctionalisation, as

    described above) (Fig. 4B). Having lost the anterior module (which

    had the potential to directly ossify) teleosts have succeeded in

    ossifying the more posterior endoskeletal component perhaps as

    functional demands required. To date, there is no evidence of

    dermal scleral ossicles arising as an atavistic structure within

    Teleostei. Interestingly, in the sister group to Osteichthyes, we have

    observed ossified plates (tesserae) within the scleral cartilage of

    several extant sharks (Pilgrim and Franz-Odendaal, 2009) and have

    documented sclerotic rings in fossil Chondrichthyes (Pilgrim and

    Franz-Odendaal, 2009). These findings suggest that Chondrichthyes

    independently evolved a mechanism to strengthen their scleral

    tissue; these mechanism(s) warrant further investigation.

    From the evidence presented above, the scleral ossicles in

    sarcoptergyians and the scleral ossicles in actinopterygians

    cannot be homologous (one is exoskeletal and one is endoske-

    letal). The scleral cartilage elements in each group (and possibly

    all vertebrates) are likely to be homologous since both are derived

    from the posterior module and share a common neural crest

    origin. Although we do not know the induction mechanism in

    each case, it is generally accepted that developmental processes

    themselves can evolve (Hall, 99). In chicken embryos, the retinal

    pigmented epithelium (RPE) has been shown to regulate the

    development of the scleral cartilage (Thompson et al., 2010) and

    these authors suggest that the RPE might direct fate choices

    within the neural crest-derived sclera. In addition, this group

    suggest an intriguing link between the development of pigmen-

    tation in the RPE and cartilage differentiation in the sclera

    (Thompson et al., 2010). In mouse embryos, Pitx2 is necessary to

    specify the fate of the neural crest-derived corneal endothelium,

    corneal stroma, and sclera (Evans and Gage, 2005) and its

    expression is induced by retinoic acid from the optic cup (Gage

    and Zacharias, 2009; Kumar and Duester, 2010). Pitx2 is also

    required for the development of ocular blood vessels, which are

    critical for the formation of chondro- and osteogenic condensa-

    tions (Evans and Gage, 2005). Another gene, Indian hedgehog

    (from blood vessels) has recently been shown to be required for

    the development of the sclera and the RPE in mouse embryos

    (Dakubo et al., 2008). Furthermore, recent findings in humans

    and rats have shown that the mammalian sclera has retained the

    ability to calcify or form cartilage (but not bone) in pathological

    situations or in response to aging (OSteen and Brodish 90; Seko

    et al., 2008). The above findings point to a shared mechanism of

    scleral cartilage induction among vertebrates.

    If the homology of the scleral cartilage across all vertebrates is

    accepted, then the different shapes of the scleral cartilage

    SCLERAL OSSICLE EVOLUTION 399

    J. Exp. Zool. (Mol. Dev. Evol.)

  • (cartilage cup vs. cartilage ring) might simply reflect different

    expression patterns of cartilage inhibitory molecules or different

    inductive potentials of the RPE (Thompson et al., 2010).

    The different mechanisms by which vertebrates have suc-

    ceeded in strengthening the ocular skeleton (e.g. birds: evolved a

    separate strengthening tissue, namely the sclerotic ring; sharks:

    evolved tesserae on their cartilage; fish: evolved a mechanism for

    perichondral ossification of the scleral cartilage) might also

    reflect evolutionary convergence.

    SUMMARY AND CONCLUSIONSThe findings presented above support our previous hypothesis that

    the scleral ossicles of teleosts are not homologous to the scleral

    ossicles of reptiles (Franz-Odendaal and Hall, 2006a). In addition,

    it further suggests that the scleral cartilage (the endoskeletal

    component of the eye) of all gnathostomes is homologous.

    The paleontological data place the earliest origin of the ocular

    skeleton to the Ordovician. Furthermore, research on the origin of

    the neural crest indicates that neural crest specifiers were present at

    this time. The developmental data conclude that the ocular skeleton

    is neural crest derived and that the endoskeletal and exoskeletal

    components of the ocular skeleton evolved independently. In

    extant reptiles, which have both exoskeletal scleral ossicles and

    endoskeletal scleral cartilage, these two independently evolving

    components have been reassociated with one another anatomically.

    Therefore considering this data, it is likely that the population

    of neural crest cells that migrates to the periocular mesenchyme

    surrounding the eye subdivided during vertebrate evolution and

    subsequently evolved independently into two distinct compo-

    nents. This subdivision occurred sometime shortly after the

    evolution of dentine and bone since the oldest known fossil

    evidence of the ocular skeleton dates to Ordovician 480440

    million years ago. This early subdivision made it possible for the

    modules to evolve independently into the diverse ocular

    skeletons we see today. In addition, since there is evidence in

    the fossil record for the presence of an ocular endoskeletal

    component alone (without the exoskeletal component) and since

    the primordial pigmented epithelium (that induces the scleral

    cartilage) evolved before the conjunctival epithelium (Lamb et al.,

    2007), it is highly probable that the endoskeletal component

    within the eye was established before the exoskeletal component.

    In conclusion, one should consider that the components of the

    ocular skeleton (cartilage and bone) likely evolved independently

    from the neural crest and that each component was patterned and

    induced by different tissues. It is especially important when

    character coding the ocular skeleton of fossil vertebrates that

    accurate terminology is used to describe this region of the skeleton.

    The problems that arise with inadequate documentation of known

    fossils was recently raised by Friedman and Brazeau (2010). The

    application of concepts such as modularity to understanding

    complex systems provides us with novel insight into their

    evolution; this insight is not immediately apparent when examin-

    ing either the paleontological or developmental literature alone.

    ACKNOWLEDGMENTSThe author thanks the Natural Science and Engineering Research

    Council of Canada (TFO, Discovery Grant) for funding this research

    and Mount Saint Vincent University who provided a student

    assistantship to Jonathon Sproul (MSVU) to collate the fossil data.

    I extend my thanks to Kathryn Knorr (MSVU) for translating the

    Edinger (1929) text from German into English. I am also extremely

    grateful to Brian Hall (Dalhousie University, Canada) for

    encouragement with this manuscript and for insightful comments.

    I also thank M. I. Coates, M. Laubichler, and P. Donoghue for

    reading earlier drafts of this manuscript. Comments from

    anonymous reviewers were very valuable and greatly appreciated.

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