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