Integrative and Comparative Biology Advance Access originally published online on May 24, 2007
Integrative and Comparative Biology 2007 47(6):865-871; doi:10.1093/icb/icm035
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Homology of ciliary bands in Spiralian Trochophores
*University of Illinois, Urbana, IL, 601 S. Goodwin, Avenue. Urbana, IL 61801, USA; University of Hawaii, Kewalo Marine Laboratory, 41 Ahui Street, Honolulu HI 96813, USA
Correspondence: 1E-mail: j-henry4{at}uiuc.edu
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A number of hypotheses have been presented regarding the origins of the metazoans and, more specifically, the Bilateria. Using various phylogenetic analyses, characteristics have been mapped on phylogenetic trees to infer ancestral body plans and life history strategies of those ancestors. Many arguments on the evolution of the Bilateria are based on the presumed homology of certain characteristics of extant larva and adults, including various ciliated bands involved in feeding and locomotion. This article considers a recent study indicating that the second, downstream-collecting, ciliated band in the veliger larva of the gastropod mollusc, Crepidula fornicata, is actually derived from secondary trochoblasts (derived from second quartet micromeres), that normally form part of the prototrochal band found in other spiralian phyla (Hejnol et al. 2007
). Despite previous arguments, these new findings suggest that the second ciliated band in the veliger larva is not homologous to the metatroch found in the trochophore larva of some other spiralians, such as the annelid, Polygordius lacteus. In the latter case, the metatroch was reported to be formed by a different set of lineage precursors (derived from third quartet micromeres) (Woltereck 1904). These findings have important implications for the interpretation of various hypotheses related to the evolution of metazoan phyla. |
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The combination of morphological comparisons, and modern molecular analyses permit one to decipher phylogenetic relationships between the extant metazoans. One can now begin to infer characteristics that define the plesiomorphic conditions of the Bilateria and Eumetazoa (Davidson et al. 1995
; Haszprunnar et al. 1995; Peterson et al. 1997, 2000; Nielsen 2003; Sly et al. 2003; Martindale 2005). Many questions can be asked, such as: did these ancestors exhibit direct (lecithotrophic) or indirect (planktotrophic) development, and did they more closely resemble the adults or the larvae of extant metazoans? Many different proposals have been put forth, but one related set of arguments that has been championed by a number of recent investigators (Jägersten 1959, 1972; Nielsen 1979, 1985, 1998, 2000, 2001, 2003, 2004, 2005; Nielsen and Nørrevang 1985; Davidson et al. 1995; Peterson et al. 1997, 2000), has close affinities to the "biogenetic law," originally proposed by Ernst Haeckel (1866, 1874). Haeckel's biogenetic law stated that, "ontogeny recapitulates phylogeny". Basically, Haeckel proposed that one could discern an evolutionary sequence of earlier adult stages in the series of transient developmental stages displayed by descendant, extant metazoans. As many embryos pass through discrete stages of cleavage, blastula formation, and gastrulation, Haeckel felt that such stages must represent sequential adult states reached by ancestral metazoans and coined terms such as "Blastaea" and "Gastraea" to describe various ancestral body plans. This idea was subsequently extended by Hatschek (1878), who proposed the existence of a descendent of the Gastraea, called the "Trochozoon," which represented a bilaterally symmetrical, ciliated, feeding adult stage that resembled the trochophore larvae of extant annelids such as Polygordius lacteus and the adults of some rotifers such as Trochosphaera aequatorialis. Subsequently, Jägersten (1972) and Nielsen and Nørrevang (1985) modified these ideas and proposed their own "Bilaterogastraea" and "Trochaea" hypotheses, respectively. More specifically, Nielsen and Nørrevang (1985, Nielsen, 1997, 1998, 2000, 2001, 2003) proposed that the trochophore larva represents the ancestral feeding larva of the Spiralia and possibly of the protostomes, in general. The Spiralia represent a large clade of protostome phyla (within the Lophotrochozoa) that include the Mollusca, Annelida (including Vestimentifera and Pogonophora as the Siboglinida, and Echiura and possibly Myzostoma), Sipunculida (also likely derived annelids), Gnatostomulida, Nemertea, dicyemid Mesozoa, and some Platyhelminthes, including polyclad Turbellaria, Catenulida, and Macrostomida.
The trochophore is the characteristic larval type found in some spiralians, including: annelids, molluscs, sipunculids, and echiurids (the later likely represents a group of derived annelids) (McHugh 1997; Rousset et al. 2007). In the trochophore, the principal locomotory ciliated band is the "prototroch" that encircles the larvae between the anterior pretrochal region located just anterior to the ventral mouth, and the more posterior or postrochal region (Fig. 1A). The cilia of the prototroch beat in a downstream (posterior) fashion, propelling the larva in an anterior direction and moving food particles towards the mouth and posterior end of the larva.
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Spiralian embryos exhibit highly stereotypic patterns of cell cleavage and a specific nomenclature has been designed to identify individual blastomeres (Conklin 1897
). Therefore, it is possible to assess the embryonic origins of specific larval and adult structures. In spiralians, the first and second cell divisions generate four blastomeres, termed A, B, C, and D (Fig. 2A and B). Each of these cells subsequently divides to form a series of smaller micromeres, formed as individual "quartets" (Fig. 2C–F). The first quartet is present at the 8-cell stage and these smaller animal pole "micromeres" are called, 1a, 1b, 1c, and 1d, while the typically larger vegetal macromeres are called, 1A, 1B, 1C, and 1D. Following this third division, three additional quartets of micromeres are born. The second quartet being called 2a–2d, the third, 3a–3d and the fourth, 4a–4d. These cells exhibit consistent patterns of development and there is a tremendous degree of homology in terms of the ultimate larval and adult fates generated by these cells in various spiralians.
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The ciliated prototroch is derived from specialized founder cells call "trochoblasts" and these are typically organized in rings derived from three sets of ciliated cells, the "primary trochoblasts," the "accessory trochoblasts," and the "secondary trochoblasts" (Fig. 1B). Close examination of the cell lineage of the prototroch in a number of species (primarily annelids and molluscs) indicates that these prototrochal cells are derived from a highly conserved set of embryonic founder cells (Table 1). The large primary trochoblasts are derived from the first quartet micromeres, 1a–1d (or more specifically vegetally placed derivatives, called 1a2–1d2). The accessory trochoblasts are also derived from the first quartet micromeres, 1a–1d (or more specifically their animal derivatives, called 1a1–1d1). Finally, the secondary trochoblasts are derived from the second quartet micromeres, 2a–2d (or more specifically their more animally positioned derivatives, called 2a1–2d1). Interestingly, the presence of a prototroch has been recently demonstrated in yet another group of spiralians, the paleonemertean, Carinoma tremophoros (Table 1, Maslakova et al. 2004
).
Other types of ciliated bands may also be present in the trochophore, such as the metatroch, gastrotroch (neurotroch), and telotroch that are variably involved in feeding and locomotion (Fig. 1A). For instance, in some species a second downstream-collecting ciliated band, called the metatroch, may be present. This band is positioned just posterior to the mouth and the prototroch, and is typically involved in feeding. The metatroch beats in the opposite direction from the prototroch, and establishes a counter-current, which together with its closely spaced cilia, traps food particles subsequently transported to the mouth by an intervening ciliated food groove (Riisgård et al. 2000). This mechanism of feeding (involving both the prototroch and the metatroch) is referred to as "opposed band feeding" (Strathmann 1978). Opposed band feeding has only been documented clearly in the larvae of some gastropods, bivalves, annelids, and echiurans (Strathmann 1987, 1993; Strathamnn et al. 1972; Emlet and Strathmann 1994; Miner et al. 1999) and an adult rotifier (Strathmann et al. 1972).
Previously, a published cell lineage for the metatroch only existed for a single annelid, P. lacteus (Woltereck 1904). Woltereck (1904) claimed that the metatroch of P. lacteus is derived from the third quartet micromeres, 3c and 3d (Table 2). Although Woltereck's analyses appears to be a very careful one, it was not done with the aid of modern cell-autonomous lineage tracers and, in fact, Nielsen (2004) doubted that assessment. Nielsen (2004) argued, that the ciliated cells Woltereck (1904) interpreted as belonging to the metatroch are likely to belong to the adoral ciliated zone. Rather, Nielsen (2004) suggests that the metatroch is derived from the second quartet micromeres, likely derivatives of 2d. This interpretation is consistent with the Trochea hypothesis and Nielsens (1979, 2001) proposal that the feeding and locomotory cilated bands (i.e., prototroch, metatroch, and teletroch) are derived from a common set of embryonic precursors that originally generated a sole ancestral ciliated band, the "archeotroch." The Trochaea hypothesis postulates that the single ancestral archeotroch would have ultimately given rise to other ciliated bands through developmental changes associated with the evolution of the Bilateria/Protostomia, involving formation of the through-gut, and ventral displacement of the mouth (e.g., protostome), and the division of the mouth and anus presumably through a process akin to that of amphistomy (Arendt and Nübler-Jung 1997; Lartilott et al. 2002; Malakhov 2004). Hence, this scheme argues for related/homologous origins of the major trochophore ciliated bands, such as the prototroch, and metatroch. Nielsen and Nørrevang (1985), and Nielsen (2001) argued that the association of the prototroch and the metatroch with opposed-band feeding represents the ancestral state in the Spiralia. On the other hand, a number of authorities disagree with this hypothesis. Some have argued that various trochophores and "trochophore-like" larvae are derived (Salvini-Plawen 1980; Heimler 1988; Ivanova-Kazas 1985a, 1985b, 1985c; Popkov 1993; Haszprunar et al. 1995; Rouse 1999, 2000a, 2000b). Rouse's (1999, 2000a, 2000b) analyses indicate that various ciliary bands have arisen via different evolutionary paths. He pointed out that opposed-band feeding and even the presence of the metatroch are not found in most Spiralia/Trochozoa, and his studies show that, in fact, the proposed likelihood for a general trend in the evolutionary loss of feeding larvae (and hence cilliary feeding structures, e.g., the metatroch) is just as great as is the gain of feeding larvae (McEdward and Janies 1997).
The veliger larva represents a typically planktonic, feeding larval stage of gastropods and bivalve molluscs. Significantly, evidence suggests that the larvae and downstream-feeding evolved independently in these two classes of molluscs (Haszprunar et al. 1995; Ponder and Lindberg 1997; Waller 1998; Zardus and Morse 1998). In both cases, veliger larvae have bilateral pairs of prominent velar lobes that possess ciliary bands located at their periphery (Fig. 1C and D). These bands function in both locomotion and feeding. The more anterior, primary ciliated band encircles the outermost edge of the large velum. Its cilia beat in a downstream direction and propel the animal through the water. A secondary ciliary band is located just posterior to the primary band that beats in the opposite direction, trapping food particles that are subsequently directed to the mouth by an intervening ciliated food groove. Veliger larvae, therefore, utilize a mechanism of opposed band feeding (Strathmann 1987). McMurrich (1885, 1886) was the first to publish speculation that the primary and secondary ciliary bands of the velum are homologous with the prototroch and metatroch of annelid trochophore larvae (Jägersten 1972; Nielsen 2001, 2004).
Obviously, these hypotheses, including the Trochaea hypothesis, are based on the presumed homology of certain larval structures, such as the ciliary bands. Careful analyses of the cell lineage can help establish whether or not such structures are derived from similar embryonic founder cells, and thus likely to be homologous.
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Recently, we conducted an analysis of the cell lineage of the gastropod, Crepidula fornicata (Hejnol et al. 2007
). This analysis employed microinjection of cell-autonomous fluorescent lineage tracers and confocal 3D-reconstruction of larval anatomy. The findings clear up a number of inconsistencies between the fate map proposed by Conklin (1897) and those generated for other molluscs (Render 1991, 1997; Dictus and Damen 1997; Damen and Dictus 2002). The results indicate that, in fact, the primary ciliary band (or protrotroch) is derived from the derivatives of the 1a–1d first quartet micromeres (specifically primary trochoblasts from 1a2–1d2, with accessory trochoblasts also being derived from 1a–1d), similar to the situation found in other trochozoans; however, the secondary ciliary band (or metatroch) is derived from the second quartet derivates 2a and 2c, with the intervening ciliated food groove derived from 2b (Table 1, Hejnol et al. 2007). These results suggest that the metatroch of C. fornicata is not directly homologous with the metatroch present in the trochophore of the annelid Polygordius (Woltereck 1904). In fact, secondary trochoblast cells appear to have been co-opted to give rise to the metatroch and food groove in the Crepidula veliger larva. These findings are, hence, in agreement with arguments proposed by Rouse (1999, 2000a, 2000b), as mentioned earlier.
As mentioned earlier, Nielsen (2004) suggested that the metatroch of Polygordius might not be derived from third-quartet micromeres, but rather from another lineage, specifically 2d. We found no contribution of the 2d lineage to the formation of any of the ciliated bands in C. fornicata. It is possible, however, that other second-quartet derivatives may generate the metatroch in other spirailians, such as P. lacteus, and this would then be more consistent with the Trochaea hypothesis presented by Nielsen (2004, 2005). Obviously, the cell lineage of P. lacteus should be reassessed using modern cell-lineage tracers and additional taxa need to be examined to resolve these fundamental issues. It is also possible that there is tremendous flexibility in the development and evolution of these structures. For instance, there is a unique, albeit minor, contribution made by 3d to the formation of the prototroch (forming secondary trochoblasts) in the chiton, Chaetopleura apiculata (Henry et al. 2004).
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This material is based upon work supported by the National Science Foundation under Grant number IOB 05-16799 to J.Q.H. (J.J.H). A.H. received support by the German Research Foundation (DFG HE5183/2-1). This material is also based on work supported by the National Science Foundation AToL program to M.Q.M.
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From the symposium "Integrative Biology of Pelagic Invertebrates" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
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