Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria

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  • Apical organs in echinoderm larvae: insights into larval evolution in the

    Ambulacraria

    Maria Byrne,a, Yoko Nakajima,b Francis C. Chee,a and Robert D. Burkec

    aDepartment of Anatomy and Histology, F13, University of Sydney, NSW 2006, AustraliabDepartment of Biology, Keio University, Yokohama 223-8521, JapancDepartments of Biochemistry and Microbiology, University of Victoria, 3800 Finnerty Road, Victoria, BC, Canada V8W 3N5Author for correspondence (email: mbyrne@anatomy.usyd.edu.au)

    SUMMARY The anatomy and cellular organization ofserotonergic neurons in the echinoderm apical organexhibits class-specific features in dipleurula-type (auricularia,bipinnaria) and pluteus-type (ophiopluteus, echinopluteus)larvae. The apical organ forms in association with anteriorciliary structures. Apical organs in dipleurula-type larvae aremore similar to each other than to those in either of the pluteusforms. In asteroid bipinnaria and holothuroid auricularia theapical organ spans ciliary band sectors that traverse theanterior-most end of the larvae. The asteroid apical organ alsohas prominent bilateral ganglia that connect with an apicalnetwork of neurites. The simple apical organ of the auriculariais similar to that in the hemichordate tornaria larva. Apicalorgans in pluteus forms differ markedly. The echinopluteus

    apical organ is a single structure on the oral hood betweenthe larval arms comprised of two groups of cells joined by acommissure and its cell bodies do not reside in the ciliaryband. Ophioplutei have a pair of lateral ganglia associatedwith the ciliary band of larval arms that may be the ophiuroidapical organ. Comparative anatomy of the serotonergicnervous systems in the dipleurula-type larvae of theAmbulacraria (Echinodermata1Hemichordata) suggests thatthe apical organ of this deuterostome clade originated asa simple bilaterally symmetric nerve plexus spanningciliary band sectors at the anterior end of the larva. Fromthis structure, the apical organ has been independentlymodified in association with the evolution of class-specificlarval forms.

    INTRODUCTION

    Nervous system organization forms the basis for description

    of body plans across the metazoa. This has generated long-

    standing interest in the links between neural anatomy, neuro-

    genesis, phylogeny, and metazoan evolution (Garstang 1894;

    Lacalli 1994, 2005; Hay-Schmidt 2000; Nielsen 2005). Here,

    we assess evolution of the echinoderm serotonergic nervous

    system with respect to larval morphology and phylogenetic

    relationships in the Ambulacraria (Echinodermata1Hem-

    ichordata), a monophyletic clade sister to the other major

    deuterostome clade (Tunicata1Chordata) (Zeng and Swalla

    2005; Swalla 2006). In echinoderms, serotonin is a conspic-

    uous marker for the bilateral larval nervous system that de-

    velops in association with the ciliary bands (Cisternas and

    Byrne 2003; Nakajima et al. 2004a; Byrne et al. 2006; Nakano

    et al. 2006).

    Our current understanding of the serotonergic system of

    echinoderm larvae is largely based on studies of seven

    echinoid (Bisgrove and Burke 1986, 1987; Bisgrove and Ra

    1989; Thorndyke et al. 1992; Nakajima et al. 1993, 2004a;

    Yaguchi et al. 2000; Beer et al. 2001) and ve asteroid (Burke

    1983a; Nakajima 1988, 2004a; Moss et al. 1994; Chee and

    Byrne 1999a) species. These studies provide an extensive da-

    taset encompassing larvae from major echinoid and asteroid

    taxa. We also have information on the serotonergic system of

    three holothuroid and one ophiuroid species (Burke et al.

    1986; Cisternas et al. 2001; Cisternas and Byrne 2003; Byrne

    et al. 2006; Nakano et al. 2006). The serotonergic system of

    the tornaria larva from the sister taxa, the Hemichordata, is

    also described (Nakajima et al. 2004b; Nezlin and Yushin

    2004; Nielson and Hay-Schmidt 2007).

    Despite their disparate adult body plans, echinoderms and

    hemichordates are united by possession of similar dipleurula-

    type larvae (Fig. 1), a feeding larval form considered to be a

    synapomorphy for the Ambulacraria (Zeng and Swalla 2005).

    Echinoderms have a diverse array of dipleurula and pluteal

    larval forms (review, Ra and Byrne 2006). Holothuroids,

    asteroids, and crinoids have dipleurula-type larvae whereas

    echinoids and ophiuroids have pluteal-type larvae with larval

    arms supported by skeletal rods (Fig. 1). The Ambulacraria is

    in an informative phylogenetic position to contribute to our

    understanding of neural evolution in the invertebrate deut-

    erostomes and in the chordates. Here, we determined if the

    EVOLUTION & DEVELOPMENT 9:5, 432445 (2007)

    & 2007 The Author(s)

    Journal compilation & 2007 Blackwell Publishing Ltd.

    432

  • Fig. 1. Phylogenetic relationships in the Ambulacraria (Echinodermata1Hemichordata) (after Smith et al. 2004) and larval forms. Theancestral dipleurula larva proposed by Muller (1853) and drawn by Dawydo (1928) is placed in a basal position. Hemichordates, crinoids,asteroids, and holothuroids have dipleurula-type larvae. Ophiuroids and echinoids have pluteal-type larvae. Serotonergic apical organs (inred) of feeding larvae and associated ciliary bands (gray bands) are shown in the schematics on the right. These sketches are made from aperspective of looking at the anterior end of the larva with the larval body projecting into the plane of the page. Crinoids do not havefeeding larvae but have a dipleurula-like ciliary band (Nakano et al. 2003) and the doliolaria, with its apical catecholaminergic cells (Chia etal. 1986), are included to complete the tree. In the holothuroid auricularia, asteroid bipinnaria and hemichordate tornaria apical organ cellbodies are located in the ciliary band nerve and give rise to bers that span between the bands. The bipinnaria also has lateral ganglia(arrows). The cell bodies of the echinopluteal apical organ are not located in the ciliary band nerve. The echinoid apical organ has twogroups connected by a bundle of nerves. In ophiuroids the apical organ of the ophiopluteus has two lateral ganglia with few cell bodieswithin the ciliary band nerve.

    Echinoderm apical organ evolution 433Byrne et al.

  • morphological similarities among dipleurula larvae extend to

    their serotonergic nervous systems and apical organs. Interest

    in the echinoderm and hemichordate larval nervous systems

    has focussed on Garstangs (1894) hypothesized evolutionary

    link between the dipleurula larva and the chordate nervous

    system. This hypothesis, that the dipleurula ciliary band was a

    forerunner of the chordate nerve cord, now has little support,

    but as the chief site of larval neurogenesis, their potential

    signicance to chordate neural evolution remains of interest

    (Lacalli 2003, 2005).

    Anterior serotonergic structures, variously called apical

    ganglia, anterior ganglia, or apical organs, are prominent in

    Ambulacraria larvae and are focal structures for comparative

    anatomy (Lacalli 1994; Lacalli and Kelly 2002; Nakajima et

    al. 2004b; Nezlin and Yushin 2004). We use the term apical

    organ. Echinoderm apical organs are well placed to serve as

    sensory structures as the larvae swim anterior end foremost

    (Burke 1983b; Bisgrove and Burke 1986, 1987; Chee and By-

    rne 1999a; Beer et al. 2001; Yaguchi and Katow 2003; Nielsen

    2005). Functional data are sparse, but some physiological and

    pharmacological studies indicate a role for serotonin in mod-

    ulation of the ciliary beat and metamorphosis (Chee and By-

    rne 2001; Yaguchi and Katow 2003; Katow et al. 2004, 2007).

    With the improved resolution aorded by confocal mi-

    croscopy, detailed comparative data on the serotonergic sys-

    tems are available for larvae of echinoderm classes that

    diverged over 500Ma (Chee and Byrne 1999a, b; Byrne and

    Cisternas 2002; Nakajima et al. 2004a; Byrne et al. 2006;

    Nakano et al. 2006). Here we review the apical organs of

    larval Echinodermata, comparing anterior serotonergic struc-

    tures in each of the classes with those in the Hemichordata.

    New data are presented for the nervous system of asteroids

    and ophiuroids. Although a focus on the serotonergic system

    considers just one subset of larval neurons, this is the only

    neurochemical for which we have good comparative data.

    Serotonin immunoreactivity has been an important anatom-

    ical tool to visualize nervous systems across the metazoa. This

    evolutionary ancient neurotransmitter is present in the ner-

    vous systems of most bilaterians from lower invertebrates to

    craniates and has received particular attention for phyloge-

    netic comparisons (Hay-Schmidt 2000; Page and Parries 2000;

    Page 2002; Nielsen 2005; Stach 2005).

    Morphological evolution of the serotonergic neurons of

    the apical organs of echinoderm and hemichordate larvae is

    assessed within a phylogenetic framework (Fig. 1). We con-

    sider the relationships among the echinoderm larval types and

    features of the putative ancestral-type neuronal organization

    in the Ambulacraria and how this organization may have

    been modied through evolution of the larval form. For the

    Echinodermata the apical organs of the asteroid bipinnaria

    and holothuroid auricularia are modern representatives of

    the ancestral-type dipleurula larva, whereas the apical organs

    of the ophiopluteus and echinopluteus represent the pluteus

    larva (Fig. 1, Table 1). The serotonergic apical organ of the

    hemichordate tornaria (Nakajima et al. 2004b; Nezlin and

    Yushin 2004; Nielson and Hay-Schmidt 2007) is also con-

    sidered. With the assumption that the dipleurula is an Am-

    bulacraria synapomorphy, we hypothesized that apical

    organs in dipleurula-type larvae should be more similar to

    each other than to these structures in pluteal forms and that

    the ancestral-type echinoderm serotonergic system was mod-

    ied independently in the dierent classes through evolution

    of larval form.

    DIPLEURULA-TYPE LARVAE

    Class Asteroidea

    Development of the asteroid serotonergic nervous system

    is rst evident in gastrulae where immunoreactive cells are

    scattered through the ectoderm of the animal half of the

    embryo (Fig. 2, A and B). In early bipinnaria these immuno-

    reactive cells appear to migrate to the mid-larval region and

    appear to line up along the developing pre- and postoral

    ciliary bands (Figs. 2, C and 3A). Bipinnaria have two ciliary

    bands (Figs. 1 and 3, A and F). Serotonin immunoreactivity

    is most evident in the anterior half and oral region of the

    larva (Fig. 3, AD). The asteroid apical organ comprises a

    network of neurites at the anterior end of the larva (larval

    apex) and two lateral ganglia at the base of the preoral hood

    (Figs. 1 and 3, C, D, and F). This structure is described for

    bipinnaria from two major asteroid orders (Fig. 3, AG),

    although the presence of the apical plexus varies among

    species. At the anterior end of the larva the pre- and postoral

    ciliary bands traverse the preoral hood parallel to each other

    on the dorsal and ventral sides of the larva (Fig. 3, A and F).

    In this region, serotonergic cells are scattered along the cili-

    ary band and bers span between the bands (Fig. 3, A and

    F). Nerve bers from cells at the larval apex extend poste-

    riorly along the ciliary band nerve to connect with the lateral

    ganglia (Figs. 1 and 3, A and D).

    In apical view, the similar development of serotonergic

    neurons along the two ciliary bands conveys a dorso-ventral

    symmetry to the apical organ (Fig. 3, A and F). The lateral

    ganglia are the most conspicuous feature of the asteroid apical

    organ (Fig. 3, BE). Fully developed ganglia have 3050 cells

    that give rise to projecting bers with a beaded appearance

    (Fig. 3, D and E). These connect with serotonergic cells in the

    oral region (Fig. 3A). Confocal imaging revealed that some of

    the apical organ cells in Patiriella regularis had cilia-like pro-

    cesses extending from their apex. These processes, about

    15mm long (SE50.03mm; n510), extend beyond the epi-thelium (Fig. 3, F and G). They may correspond to the sen-

    sory-like process identied in ultrastructural studies of the

    apical organs of the bipinnaria of Pisaster ochraceus (Lacalli

    et al. 1990). At their base, these cells give rise to bers with a

    beaded, varicose appearance (Fig. 3G).

    434 EVOLUTION & DEVELOPMENT Vol. 9, No. 5, September^October 2007

  • As the bipinnaria develop to the settlement-stage bra-

    chiolaria larva, the anterior serotonergic cells appear to

    disperse along the ciliary band nerve tracts. Brachiolaria

    have three brachial arms and an adhesive disk for benthic

    attachment (Fig. 3H). The lateral ganglia seen in the bipinn-

    aria are conspicuous in the brachiolaria of Asterina pectinif-

    era, but are absent in the competent brachiolaria of

    P. regularis (Fig. 3H). Settlement-stage larvae of P. regularis

    have serotonergic neurons in the epithelium of the bra-

    chial arms. There are no traces of the apical organ in

    lecithotrophic asteroid larvae and these larvae also lack

    ciliary bands (Fig. 3I). Lecithotrophic brachiolaria have

    serotonergic cells in the adhesive papillae of the brachiolar

    arms (Fig. 3, I and J) that have cilia-like apical processes and

    basal neurites (Chee 2000).

    Class Holothuroidea

    In holothuroid development, serotonin-positive cells rst

    appear at the animal pole of late gastrulae where they

    develop into the apical organ (Byrne et al. 2006; Nakano et al.

    2006). Early serotonergic cells remain at the anterior end of

    the developing auricularia and become aligned along the an-

    terior ciliary band region. Holothuroid auriculariae have

    a single ciliary band that loops around the body and two

    portions of the band traverse the right and left sides of the

    larval apex (Figs. 1 and 4A). These two bands are oset 901compared with those that cross this region in the asteroid

    bipinnaria (cf. Figs. 3A and 4A). The arrangement of the

    ciliary band of the auricularia is similar to that in the tornaria

    larva of hemichordates (Fig. 1).

    Unlike asteroids, early serotonergic cells do not migrate

    in the auricularia as the ciliary band forms. Serotonin

    immunoreactivity remains restricted to the anterior-most

    region of the auricularia (Fig. 4, AD). The apical organ of

    Chirodota gigas develops as two groups of serotonergic neu-

    rons associated with the right and left anterior ciliary band

    sections at the larval apex with a few processes connecting the

    bands (Fig. 4, AD). Similar apical nerve connections are

    described for the auriculariae of Parastichopus californicus

    and Stichopus japonicus (Burke et al. 1986; Nakano et al.

    2006). These three species represent two major holothuroid

    orders. Ganglionic clusters of serotonergic cells do not devel-

    op in auriculariae. In C. gigas, six to 22 serotonergic cells

    develop along the apical ciliary band sectors and a few bers

    span between them in the short stretch where the bands run

    parallel to each other (Fig. 4, C and D). The cells are bipolar

    and multipolar and are interconnected by processes. A few

    immunoreactive cells present in the oral hood connect with

    the ciliary band nerve (Fig. 4, A and B). Bipolar sensory

    cells that may correspond to serotonergic cells are present in

    the anterior ciliary band region of aur...

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