Ciliary Bands in Echinoderm Larvae: Evidence for Structural Homologies and a Common Plan
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Acta Zoologica (Stockholm), Vol. 74, No. 2, pp. 127-133, 1993 Printed in Great Britain
0001-7272/93$6.00+ Pergamon Press Ltd .OO
0 1993 The Royal Swedish Academy of Sciences
Ciliary Bands in Echinoderm Larvae: Evidence for Structural Homologies and a Common Plan
T. C. Lacalli Biology Department, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N OW0
(Accepted for publication 27 April 1992)
Lacalli, T. C. 1993. Ciliary bands in echinoderm larvae: evidence for structural homologies and a common plan.-Acta Zoologica (Stockholm) 74: 127-133.
A series of laterally projecting ridges develop along the ciliary band of late stage auricularia larvae. These are similar in position to the larval arms of bipinnaria larvae and the epaulettes and vibratile lobes of echinoid pluteus larvae, all of which structures are potentially homologous. When the auricularia is converted to a doliolaria with a series of circumferential ciliary bands, the ridges of the former are retained as basic elements from which the circumferential bands of the latter then develop. There is a simple repeating pattern in the arrangement of these elements in which bands composed of two elements alternate with bands composed of four. The available evidence does not resolve the question of which of the above four larval types, whether feeding or non-feeding, is more primitive. The common plan apparent among them suggests, however, that this plan, whatever its origin, predates the diversification of larval types among eleutherozoan echinoderms.
Thurston C. Lacalli, Biology Department, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N OWO.
Echinoderm larvae are diverse morphologically, but have long been recognized as variants of a common plan (Miiller 1853). The circumoral feeding band is clearly homologous among the planktotrophic larvae of eleu- therozoan echinoderms, i.e. the pluteus, bipinnaria and auricularia, but has been modified with the evolution of various projecting lobes, ridges and skeletally supported arms in these larvae. These structures are variously named in the different larvae, based on their position on the larval body, and there is a tacit assumption in at least some instances that similarly positioned structures are, or may be, homologous. This assumption has seldom been explicitly examined. To do so on the basis of classical accounts, in the literature, means coping with the limi- tations of light microscopy and two-dimensional line drawings. These seldom show the spatial relationships between structures very clearly. Scanning electron microscopy (SEM) provides more meaningful information on the three-dimensional relationships between struc- tures, and can be used to advantage, as this paper illus- trates, in comparative studies of larval organization.
This study deals with the regional differentiation of the ciliary band in the auricularia larva into a series of ridge- like elements that persist in the doliolaria. A more detailed account of the morphogenetic process will be published separately. For the purposes of this paper, it is sufficient to examine the initial and final stages of this process, in order to identify basic patterns for comparison with other eleutherozoan larvae. The evolutionary impli-
cations of the results are discussed, but a number of unresolved questions remain.
This account is based on studies of cultured larvae of three species: Strongylcentrotus franciscanus (A. Agassiz), Piraster ochraceus (Brandt), and Stichopus californicus (Stimpson). The cultures were maintained by Dr T. H. J . Gilmour, who kindly provided larvae at various stages for EM fixation, and also prepared the specimens shown in Fig. 4. The rearing methods have been previously described (Gilmour 1985, 1988), and in all cases the larvae shown are from cultures that metamorphosed successfully. This is important in assessing the normalcy of their appearance, particularly in the case of the auricularia and doliolaria larvae, since abnormalities are common in these under all but optimal conditions. Cultured larvae of Holothuria mexicana Ludwig (see Lacalli 1988) and Lytechinus pictus (Verrill) were also examined as part of this study, but are not figured or discussed in detail.
For SEM, larvae were first relaxed in a 1:l mixture of isotonic MgCI, and sea water and then fixed by the semi-simultaneous method as described by Lacalli & West (1986). They were then critical-point dried, fixed to stubs, and examined using a Philips 505 SEM.
(a) A uricularia larvae
Figures 1 and 2 together show how the ciliary band reor- ganizes during the auricularia-to-doliolaria transition in Stichopus californicus. Smiley (1986) gives an excellent
128 T. C. Lacalli
Fig. 1 . Srichopus ca1ifornicus.-A. A late-stage auricularia in oblique ventral view. Shows the preoral and postoral transverse bands (rb) which conceal the mouth. The lateral portion of the ciliary band, on each side, is developed into a series of projecting ridges: the ventral preoral @ r ) , postoral (Po), anterior-dorsal (ad), mid-dorsal (md) posterior-dorsal @d) , and posterior-lateral @r) ridges, and an additional ridge-like element along the anterior preoral margin ( u p ) of the preoral loop of the band.-B. Doliolaria stage, same scale as (A) with five circumferential bands (numbered) nearing completion. The anterior opening (*) leads to the vestibule and mouth. A remnant of the larval anus is visible between bands 2 and 3.-C, D. Initial and intermediate stages in the morphogenetic transformation; osmium-stained specimens. The five pairs of hyaline spheres form in association with the anterior, dorsal and posterior ridges. They are visible here as dark spots, and as dark shadows in (A). Arrows indicate the right preoral ridge, which is retained in the doliolaria. Its counterpart on the left side disappears. Scale bars 200 pm.
description of morphogenesis as a whole for this species, but with emphasis on internal changes rather than exter- nal ones. Holothuria mexicana shows the same pattern of external changes as S. californicus.
In the late stage auricularia, the convoluted circumoral band forms a series of projecting ridges (Fig. 1A). The direction of cilium beat all along the band is away from the oral field (arrows in Fig. 2A), and the ridges are disposed in such a way that their cilia beat predominantly posteriorly. They thus provide the major part of the locomotory force required to move the larva forward. The functional importance of this arrangement is dis- cussed more fully by Strathmann (1971; see also Emlet 1991). The auricularia has seven pairs of ridges in total, arranged in a bilaterally symmetric fashion. Three are dorsal: the anterior-dorsal, mid-dorsal and posterior-dor- sal ridges (ad, md, andpd, respectively, in Fig. 1A). Two are ventral: the preoral and postoral ridges (pr and po in Fig. 1A); and the anterior margin of the preoral portion
of the band forms what is effectively a third, but less pronounced anterior preoral pair of ridges (upr in Fig. 1A). Last, and most posterior, is the posterior-lateral pair of ridges (p l in Fig. 1A). When the auricularia con- verts to a doliolaria (Fig. lB), portions of the auricularia band are retained, as shown in Fig. 2. What seems to be overlooked in published accounts is that the retained portions are not simply arbitrarily positioned segments of the band, but are specifically those parts of the band already recognizable as ridge-elements. Intervening seg- ments of the band are resorbed and disappear.
The reorganization process can be understood by care- ful examination of Fig. 2. The posterior rearrangements are the easiest to follow, and the results reported here agree with previous accounts where these are concerned.
The most posterior band, band 4, develops in a straight- forward way by elongation and fusion of two lateral elements, each derived from one of the posterior-lateral ridges of the auricularia. Each lateral half of band 3 comes
Comparing Echinoderm Larvae 129
Fig. 2. Summary diagrams of the auricularia-to-doliolaria transition in S. californicus showing the origin and positional shifts of the band segments retained by the doliolaria. ( A ) and (C) are tracings of Figs 1A and B, respectively, while ( B ) shows an intermediate stage seen in the same orientation as (A). Band segments are designated by band number, whether left ( L ) or right ( R ) side, and position, whether ventral ( v ) , dorsal ( d ) or lateral (la?). Arrows show the direction of cilium beat in (A), and the direction of beat this would produce in (C) assuming no cellular reorientation occurs within the individual band segments.
from two elements: the ventral postoral ridges and the mid-dorsal one on each side. Altogether, four elements are required. All four lie roughly at the same anteropos- terior level with respect to the body axis, but their connec- tion to each other is established only after their original connections with the rest of the circumoral band are broken. The three pairs of elements that form bands 3 and 4 are good landmarks for comparison between larvae. On each side, the ventral-postoral, posterior-dorsal and posterior-lateral ridges form an inverted triangle with the posterior-lateral ridge at the lower vertex. This arrange- ment is conserved in the bipinnaria and in the pluteus (cf. Figs 4, 5C).
Choosing a meaningful numbering system for the doli- olaria bands is problematic. Doliolaria larvae occur in both holothurians and crinoids, and typically have either four or five bands. The convention used here, numbering the bands M, is chosen to facilitate comparison with crinoid larvae, so the four posterior-most elements corre- spond. Crinoid larvae typically have four complete bands (e.g. Lacalli & West 1986), but an additional apical, often partial band-like element occurs in some species. Posterior structures seem in general to be less modified in echinoderm larvae than anterior ones, although the posterior half of a larva can be substa.itially altered in terms of overall shape by the addition of new structures, as in the case of the pluteus (see below).
Band rearrangement in S. californicus is asymmetrical. As shown in Figs lC, D, and 2, only the right preoral ridge is retained. It becomes the medial element of band 1 in the doliolaria, as also occurs in H . mexicana. The remainder of band 1 comes from the paired anterior dorsal ridges. All the other bands in both species are formed in a bilaterally symmetrical fashion: band 2 resembles band 4 in that it forms from a single pair of lateral elements, while band 3 is formed from two pairs of elements as described above. The observed asymmetry is probably a secondary condition, which means band 1 may originally have been derived from four elements in much the same manner as band 3. This suggests a basic plan, shown in schematic form in Fig. 3 in which bands composed of two elements alternate with bands composed of four, the 2:4:2:4:2 plan referred to in the Discussion.
Note from Fig. 2 that for all the bands except band 0, if the cilia in each band segment retain their original orientation, they will automatically beat in the correct direction in the doliolaria, i.e. posteriorly. This can in fact be seen in Fig. 1, because the cilia are preserved predominantly in a downstroke position. Band 0 is anom- alous in this respect. It forms from a straightforward ventral joining of the posterior ends of two band segments deriving from the two sides of the anterior preoral margin of the band. If the cilia in these band segments were to retain their original orientation, their direction of beat in the doliolaria would be toward the apex of the larva (Fig. 2C), opposite to that of the other four bands. This appears not to happen, which means that some degree of internal reorganization must occur in band 0 during morphogenesis. The significance of this observation is not clear. It conflicts with published accounts of band rearrangement in Synapfa (Metschnikoff 1869; Bury 1895). Bury takes special care to describe and figure changes involving the anterior bands. His equivalent to
130 T. C. Lacalli
(b) Bipinnariu larvae
1 'b \ &
Fig. 3. An idealized, schematic plan for the doliolaria showing the constituent elements of each band, and assuming bilateral symmetry. Band 0 has two elements, and the remaining bands then alternate between four elements and two. See text for discussion.
band 0 reverses its orientation as a whole as it moves, which avoids the problem of internal reorganization. This difference may be a real one reflecting differences between apodan larvae, of which Synapta is an example, and those of aspidochirotids, examined here. Metschni- koff's figures show that there are clear differences in the apical organization of his larvae compared with Stichopus.
Figure 4 shows two stages in the development of Pisaster ochraceus, a bipinnaria at the stage of arm initiation, and a brachiolaria with a well-developed complement of larval arms, including the three small brachilolar arms that sur- round the anterior adhesive disc. The larval arms in star- fish larvae can be long and tubular, as in this larva, or broad and flap-like. The similarity between the bipinnaria and auricularia pattern is best seen in the positioning of the postoral, posterior-lateral and posterior-dorsal elements. Compare the positioning of these three elements in the starfish (Po, p l , and p d in Fig. 4A; arrows in Fig. 4B) with their counterparts in the auricularia (Po, p l , and p d in Fig. 1A). The same inverted triangular arrangement is evident in both. The preoral elements (pr in Figs lA , 4A) are also similarly positioned. The remaining dorsal structures are more problematic. The auricularia has two pairs of dorsal ridges in addition to the posterior one (md and ad in Fig. 1A). One lies slightly anterior, the other posterior, to the position of the single pair of anterior-dorsal lobes in the bipinnaria (ad in Fig. 4A). The latter could be a composite structure, and its irregularly curved margin may be an indication that more than one ridge element has been incorporated into it. Alternatively, it could be an enlarged version of the mid-dorsal element, which means paired anterior-dorsal components are missing altogether in the starfish band. It is clear, in any event, that the anterior part of the starfish larva differs substantially from that of the auricu- laria. In particular, medial structures predominate rather than paired ones. The possible relation between the bra-
Fig. 4. Pisaster ochruceus larvae in oblique ventral view.-A. A bipinnaria showing the initials of the larval arms, labelled following the scheme in Fig. 1.-B. An older brachiolaria stage with elongate bipinnaria arms and three short brachiolar arms (ba) . Arrows indicate the ba...