© 2003 by The Society for Integrative and Comparative Biology
Bridging Morphological Transitions to the Metazoa1
1 Department of Biology, Appalachian State University, Boone, North Carolina 28608
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Our inability to answer many questions regarding the development of metazoan complexity may be due in part to the prevailing idea that most eukaryote "phyla" originated within a short period of geologic time from simple unicellular ancestors. This view, however, is contradicted by evidence that larger groups of eukaryotes share characters, suggesting that these assemblages inherited characters from a common ancestor. Because molecular analyses have had limited success in resolving the relationships of higher eukaryote taxa, we have undertaken a phylogenetic analysis based primarily on morphological characters. The analysis emphasizes characters considered to have a high probability of having evolved only once. Transitions between taxa are evaluated for the likelihood of character-state transformations. The analysis indicates that the evolutionary history of the clade containing the Metazoa has been complex, encompassing the gain and loss of a secondary and perhaps a primary photosynthetic endosymbiont with accompanying changes in trophic level. The history also appears to have included a hetero-autotrophic ancestor that possessed a "conoid" feeding apparatus and may have involved a transformation from a flagellate to an amoeboid body form, a trend toward increased intracellular compartmentation, and the development of complex social behavior. Such changes could have been critical for establishing the underlying complexity required for a rapid diversification of cell and tissue types in the early stages of metazoan evolution.
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INTRODUCTION |
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The history of eukaryotes prior to the appearance of the first recognizable animals has the potential of revealing a great deal about the origin and early diversification of the Metazoa. Elucidation of this history, however, depends on obtaining an accurate phylogeny of eukaryotes. While analyses using the small subunit (SSU) rRNA gene (Van de Peer and De Wachter, 1997
; Lipscomb et al., 1998; Philippe and Adoutte, 1998; Silberman et al., 1999; Atkins et al., 2000; Cavalier-Smith, 2000b; Kühn et al., 2000; Van de Peer et al., 2000) and protein sequences (Baldauf and Palmer, 1993; Keeling and Doolittle, 1996; Hashimoto et al., 1997; Philippe and Adoutte, 1998; Baldauf 1999; Dacks and Roger, 1999; Keeling et al., 1999; Pawlowski et al., 1999; Roger et al., 1999; Baldauf et al., 2000; Edgecomb et al., 2001; Horner and Embley, 2001; Moriya et al., 2001; Bapteste et al., 2002) support a close relationship between the Fungi and Metazoa (Opisthokonta), and actin phylogenies (Baldauf and Palmer, 1993; Philippe and Adoutte, 1998; Baldauf et al., 2000; Yamamoto et al., 2001) include mycetozoans as a sister group of the opisthokonts (see also Strechmann and Cavalier-Smith, 2002), molecular studies generally fail to resolve deeper relationships. Although the mycetozoans and opisthokonts branch closest to red and green algae and plants in many trees, bootstrap values are usually less than 50. The uncertainty seems to imply that metazoans arose in a polytomy reflecting an explosive radiation of most higher eukaryote taxa (E, Fig. 1, left). Except for the fungi, and perhaps mycetozoans, metazoans would not be directly related to other higher eukaryote taxa, and the ancestor of the opisthokonts would have varied little from the simple flagellate thought to be the ancestor of all living eukaryotes. Metazoan characters would have developed independently as autapomorphies, and character states appearing to be shared with other taxa would be convergent. Other than finding intermediates in the fossil record, it would be difficult to determine how metazoan characters arose. In the contrasting scenario, however, ancestors leading to the metazoans would have been shared with many other taxa (Fig. 1, right). Although some characters would have originated in the metazoan stem group, others would have arisen in deeper stem groups, and critical steps in the acquisition of these characters could be inferred by optimizing character states onto internal nodes.
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To help resolve the apparent polytomy in eukaryote trees we have undertaken a phylogenetic analysis using primarily morphological characters but including some molecular and biochemical characters. To resolve deeper relationships we have combined taxa into larger operational taxonomic units. The topology of the resulting tree(s) can reveal which character states are autapomorphies of metazoans and which were acquired in deeper stem groups. Thus, the relationships of the eukaryotes can reveal fresh insights into the development of characters that may have shaped metazoan diversification.
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METHODS |
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A heuristic search was conducted using PAUP* 4.0b 10 (Swofford, 2001
) with ACCTRAN optimization. Character evolution was examined using MacClade 4.0 68K (Maddison and Maddison, 2000).
Several explicit assumptions of monophyly were made for operational taxonomic units identified by protein and rDNA sequence analyses and morphology (Appendix 1). Some of these units, which include the alveolates, cercozoans, cryptomonads, euglenozoans (plus heteroloboseans), haptophytes, and ramicristates (see Patterson, 1999), encompass superphyla. Because the hyphochytrids within the stramenopiles have a nuclear cap of clumped ribosomes found elsewhere only in chytrids (Lange and Olson, 1979), they, along with slabrynthulids and bicosoecids, were considered separately from the stramenochromes (plus oomycetes) (Appendix 1). The glaucophytes, red and green algae, and plants are considered to derive from an ancestor that had a cyanobacterial endosymbiont and were placed in single taxon, the primary (1°) photobionts. The opisthokonts (including Corallochytrium, choanoflagellates, rotospherids, and ichthyosporeans) also form a single unit. Additional units include centroheliozoans and kathablepharids. The latter share key characters with other taxa and may reveal critical transitional states. Finally, two "excavate" taxa, the retortamonads (metamonads) and "core" jakobids, were also included. The diplomonads are consistently basal in both protein and rDNA trees (i.e., Bapteste et al., 2002) and the free-living "core" jakobid, Reclinomonas, has a mitochondrial genome that is the most similar among eukaryotes to the alpha-proteobacterial symbiont that gave rise to mitochondria and hydrogenosomes (Lang et al., 1997; but see Edgcomb et al., 2001). These taxa along with the euglenozoan/heterolobosean unit, whose closed pleuromitosis seems to be closest among non-obligately parasitic taxa to cell division in prokaryotes (see Raikov, 1994), served as alternate outgroups.
Many characters are morphological (mainly ultrastructural). Morphological characters provide an independent test of relationships because the forces driving morphological change are largely unrelated to those shaping the evolution of molecules currently used for phylogenetic analysis. Although unique molecular and biochemical characters were also used, protein and ribosomal DNA sequences were not included to avoid overwhelming the morphological signal with a larger set of phylogenetically informative sites or biasing support for key nodes with artifacts from unequal rates in nucleotide substitution and mutational saturation (Philippe and Adoutte, 1998; Philippe et al., 2000). The 96 characters were organized into 9 categories (flagella, basal bodies and transitional zone, rootlets and rhizoplasts, cell coverings, cortical structures, cytoplasmic organelles, mitosis and meiosis, plastids, and miscellaneous [see Appendix 1]) and were evaluated by several criteria.
1) Character states at the ancestral nodes of larger taxonomic units were found by informal optimization. Character states found in the basal members were considered to have a higher probability of representing apomorphies supporting these nodes, and hence of being more informative, than those found in more derived taxa. Because large taxa such as alveolates exhibit enormous diversity, character states were limited to those shared with other taxa.
2) Characters were evaluated on their likelihood of having arisen only once. Criteria providing a measure of uniqueness include how unusual the character is compared to related characters, its distribution, and its level of complexity. For example, because microtubular rootlets are ubiquous in flagellated and ciliated cells, exhibit enormous diversity across eukaryotes, and thus have a high potential of being convergent, different rootlet types should meet stringent criteria before being accepted as homologous character states. Moreover, although characters expressed in most taxa of a clade but not outside the clade convey unambiguous information regarding their origin, many characters have spotty distributions. Such distributions are difficult to interpret because they could indicate that characters either evolved repeatedly or that they evolved once and were lost repeatedly. Because easy to evolve characters are likely to be convergent, characters that appear to have been difficult to assemble because of their complexity probably can be considered to have evolved once and been lost repeatedly.
3) Characters were evaluated to capture their entire transformation (Fig. 2). For example, the history of the intermediate filament gene family extends from a role of anchoring chromatin within the nucleus to an intercellular support function as neurofilaments or desmosomal filaments in the cytoplasm to a protective role as the keratin fibrils of feathers and hair in warm-blooded vertebrates. Many characters, however, are defined so narrowly that transitional states outside the taxa for which they originally were described cannot be identified. However, characters evolve and undergo adaptive radiations as semi-independent entities. To capture their entire history all states must be identified and considered as likely to reflect character evolution as non-homology.
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4) The full range of expression of characters was examined to identify breaks or discontinuities among character states. Morphological discontinuities are often associated with differences in function that are in turn linked to the changes in selection that drive further morphological divergence. Some discontinuities are sufficiently large to represent gaps between characters and not merely transformations between states. Character states not directly related to each other (i.e., those not developing from a common ancestral state or from each other) may warrant full character status. For example, although both neurofilaments and the keratin in feathers are members of the intermediate gene family, they should not be coded as the same character in most analyses. However, feather-like scales and feathers may be treated as one because they can be assumed to have evolved directly from one to the other. Thus the functional history of characters and their usefulness in discriminating among taxa were assessed a priori.
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RESULTS AND DISCUSSION |
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The data matrix contained 16 taxa and 96 characters of equal weight and coded unordered (Appendix 2). The analysis found 90 parsimony-informative characters and gave a single most parsimonious tree (length = 197; CI = 0.5888; RI = 0.5888; RC = 0.3467; HI = 0.4112). These parameters did not change when the alternate outgroups were used. However, when the "core" jakobids were chosen, the euglenozoans/heteroloboseans and metamonads were more closely related to each other than either was to any other taxon.
Sister relationships are illustrated in Figures 3, 4. Phylogenetically informative characters (without *) are indicated in Figure 4. Certain characters were assigned a Dollo-up character type (*) a posteriori to capture their earliest possible origin. The opisthokonts, which encompass metazoans, are positioned on the far right as a sister group to the centroheliozoans. This position is supported by flattened mitochondrial cristae and siliceous scales having inwardly rolled longitudinal margins. In Raphidiophrys the latter character is expressed in a continuum extending from almost flat flakes to tightly rolled rods resembling monaxial spicules. Siliceous scales are formed similarily in silicon deposition vesicles in choanoflagellates (and sponges) and many other protists (Ogden and Coûteaux, 1987; Ogden, 1991). If the close relationship between centroheliozoans and opisthokonts is correct, then a similar trend in the stem group of the choanoflagellates and metazoans could have produced rods (costae) or monaxial spicules.
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The opisthokonts plus centroheliozoans are sister to the ramicristates. This relationship is congruent with analyses of proteins (Kuma et al., 1995
; Keeling and Doolittle, 1996; Roger et al., 1996; Baldauf and Doolittle, 1997; Bhattacharya and Weber, 1997). Centroheliozoans branch in this clade, not only because they share characters with opisthokonts, but also because they possess laminate, perinuclear microtubule organizing center (MTOC) in common with centramoebae within the ramicristates. In centroheliozoans laminate MTOCs function as central nucleating sites for radiating arrays of microtubules supporting axopodia. In centramoebae they organize arrays of microtubules, but axopodia are absent, suggesting they originated in a centroheliozoan-like ancestor and are retained in secondarily simplified amoebae, which then are a paraphyletic grade. Alternatively, a basal amoeboid body plan is consistent with the development of social behavior in which dispersed cells cooperate in forming a new entity as seen in certain ramicristates. The relationship is also supported by the anterior flagellum arising from the #2 basal, body. Of interest is Sorodiplophyrs, which shares branching or anastomozing mitochondrial cristae with the ramicristate but possesses a body plan, life cycle, and flattened organic scales in common with the slabrynthulids. This genus is also similar in morphology and life cycle to Corallochytrium, a taxon which groups with the metazoans in 18S trees (Cavalier-Smith and Allsopp, 1996).
The sister relationship between the clade containing opisthokonts and ramicristates and the stramenopiles is supported by Golgi with their forming face toward the nucleus and branched tubular cristae. The cercozoans form a sister group to this clade based on presence of a transitional helix, siliceous scales, and clumped ribosomes. Although the nuclear cap of clumped ribosomes was once thought to unite hyphochytrids and chytrids, molecular evidence (i.e., Ben Ali et al., 2002) places the hyphochytrids firmly in the stramenopiles and not the fungi. Nevertheless, the distribution of this character is noteworthy. Similar but smaller aggregates of ribosomes are found in cercozoans (Ogden, 1991, Figs. 8, 17; Anderson and Cowling, 1994, Figs. 10, 11) bicosoecids, ramicristates (Thomsen and Larsen, 1993), and perhaps even Colpodella (Spiromonas; Foissner and Foissner, 1984) and some haptophytes (Green, 1980, Figs. 38, 39), but comparable clumping is absent in other eukaryotes. The apparent intermediate level of expression in the above taxa and differences in its expression in chytrids and hyphochytrids suggest the character developed in parallel. Although a nuclear cap sensu stricto may have been absent in the last common ancestor of chytrids and hyphochytrids, some of the genetic underpinnings necessary for its later development could have evolved preadaptively. The genetic foundation for sequestering ribosomes near the nucleus could have developed in amoeboid or heliozoan ancestors. Organisms with extensive, perhaps reticulating or anastomozing, networks of pseudopodia are prone to frequent tears and would have been at an adaptive advantage if they could concentrate ribosomes where they would not be lost.
The cercozoans may be paraphyletic for several reasons. 1) The thaumatomonads share with the haptophytes a more derived location for scales on the anterior of two flagella, a character absent in taxa higher on the tree (stramenopiles have tripartite tubular hairs). In addition, the chlorarachniophyte Bigelowiella (Moestrup and Sengco, 2001) possesses an anterior projection reminiscent of a haptonema. 2) Both cercozoans and haptophytes have more derived types of scales. Scales in both groups are structurally close to the ones found in stramenopiles and centroheliozoans, although those in haptophytes are not siliceous. 3) Chlorarachnion, a basal cercozoan in molecular analyses, shares with the dinoflagellates a flagellum that fits into a spiral groove on the cell surface, and Bigelowiella has extrusomes or trichocytes similar to those in the alveolate Colponema.
Several characters supporting this and other nodes may describe paraphyletic grades of organization rather than clades (Table 1). For example, alveoli-like structures are found in glaucophytes and haptophytes as well as the alveolates. The box-like scales found in thaumatomonads, certain filiose testate amoebae, and haptophytes are also present in more basal prasinophytes and dinoflagellates, while more derived scales with a central rib unite the cercozoans and haptophytes with stramenochromes or centroheliozoans (Fig. 5A). In addition, the cone of microtubules nucleated on or near basal bodies and surrounding the nucleus as well as one type of transitional helix link certain cercozoans with the mycetozoans and opisthokonts while basal bodies with parallel sinuous filaments and a second type of transitional helix unite other cercozoans with the stramenopiles. Structures such as a paraflagellar rod, fine flagellar hairs, and "conoid" may also define grades of organization rather than monophyletic clades.
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The "conoid" in particular warrants notice (Fig. 5B). The conoid of apicomplexans is considered here to be the same character as the feeding apparatus of perkinsids, perhaps suctorian ciliates, and kathablepharids (Lee et al., 1991
; Clay and Kugrens, 1999a, b). The latter organisms are remarkably cryptomonad-like except for their obvious "conoid" (Lee and Kugrens, 1991; Lee et al., 1992, 1993). The "conoid" also can be compared to the peduncle of dinoflagellates (Calado et al., 1998; Larsen, 1988; Norén et al., 1999), which in turn is reminiscent of the haptonema of haptophytes. The peduncle and haptonema, however, differ in several details, including the absence of alveolae in the peduncle. These differences suggest that they developed in parallel from ancestors with projecting beak-like feeding structures similar to that found in Colpodella.
The deep branching of the cryptomonad clade and its sister relationship to a majority of the other taxa is consistent with the hypothesis that there was a single secondary endosymbiosis involving the uptake of a unicellular red alga, at least for those plastids deposited within the endoplasmic reticulum (Fig. 5C). If a single secondary endosymbiosis occurred prior to the separation of the cryptomonads, then one can predict that all descendants retaining the original secondarily derived plastid would share common plastid features. This prediction is well supported by data from all chlorophyll-c-containing plastids that are surrounded by four membranes (Saunders et al., 1995; Ohta et al., 1997; Fagan et al., 1998; Delwiche, 1999; Durnford et al., 1999; Stoebe and Kowallik, 1999; Zhang et al., 1999, 2000; McFadden, 2001; Sorhannus, 2001; Yoon et al., 2002).
What is less clear is the relationship of the three-membraned chlorophyll-c plastid of peridinin-containing dinoflagellates and the reduced plastid of the apicomplexans. Cavalier-Smith (1999) has postulated in the chromalveolate theory that all chlorophyll-c-containing plastids diverged from a common ancestor that obtained its plastid from a unicellular red alga. Support for this idea is seen in the similarity of the light-harvesting antenna proteins of the crytomonads, haptophytes, dinoflagellates, and heterokonts to those same proteins in the red algae (Durnford et al., 1999), as well as, analysis of plastid-targeted glyceraldehyde-3-phosphate dehydrogenase gene sequences (Fast et al., 2001). These results seem to support a common origin for the plastid of the cryptomonads, alveolates, haptophytes, and heterokonts (Fig. 5C).
Our results, however, only partially support the chromalveolate hypothesis. In our tree the alveolates are not a sister to the chromists as suggested by Cavalier-Smith (1999) but emerge as a sister to a large clade in which the haptophytes are the most basal taxon (Figs. 3, 4). Also contained in this clade are the cercozoans, a heterogeneous taxon that includes the chloroarachnids, which contain an endosymbiont produced by the uptake of a unicellular green alga. How can we reconcile this?
The early establishment of a chlorophyll-c-containing plastid basal to the divergence of the cryptomonads suggests that there have been multiple independent losses of plastids such as those known to have occurred within the heterokonts and alveolates (Delwiche and Palmer, 1997; Palmer and Delwiche, 1998; Cavalier-Smith, 1999, 2000a; Tengs et al., 2000; Fast et al., 2001; McFadden, 2001; Yoon et al., 2002). Several workers have suggested that the entire alveolate clade is derived from a photosynthetic ancestor and that basal non-photosynthetic dinoflagellates lack plastids secondarily (Gunderson et al., 1999; Fast et al., 2001; McFadden, 2001; Saldarriaga et al., 2001, 2002; Yoon et al., 2002). Our results would extend independent plastid loss to the ancestors of the cercozoans as well as the clade containing ramicristates and opisthokonts (Figs. 5C, 6).
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In contrast to the cabozoan theory of Cavalier-Smith (1999)
, we propose that the chlorophyll-b-containing plastids were acquired independently by secondary endosymbiosis of a green alga in the euglenozoans and cercozoans. In the case of the cercozoans the acquisition of a chlorophyll-b-containing plastid would have followed a deeper loss of the initial chlorophyll-c-containing secondary plastid. This scenario is congruent with Cavalier-Smith's (2002) recent rejection of the cabozoan theory based on the basal placement of euglenozoans in molecular trees. The later acquisition of secondary and/or tertiary plastids in euglenids and chlorarachnids is also supported by the clustering of the light-harvesting complex (LHC) proteins from Chlorarachnion and Euglena with LHCII, suggesting that endosymbiosis occurred after the development of advanced LHC in the green algal ancestor (Durnford et al., 1999). The acquisition of a secondary plastid in euglenids is also supported by the observation that plastid targeted proteins in Euglena are imported into the chloroplast as Golgi derived membrane bound precursors (Sulli and Schwartzbach, 1995, 1996; Schwartzbach et al., 1998). Furthermore, serial acquisition of different plastid types is known for other photosymbionts, namely the dinoflagellates, which seem to have acquired plastids from pigmented stramenopiles, haptophytes, and chlorophytes in addition to red algae (Kite and Dodge, 1985; van den Hoek and Mann, 1995; Delwiche and Palmer, 1997; Palmer and Delwiche, 1998; Cavalier-Smith, 1999, 2000a; Delwiche, 1999; Tengs et al., 2000).
Early acquisition of a secondary plastid of red algal origin would have allowed a protein import mechanism across the plastid membrane to develop very early in the diversification of the eukaryotes. As pointed out by McFadden (1999) this event would have been critical to successful maintenance of the symbiont once endosymbiontic gene sequences were transferred to the host nucleus. The presence of a similar system for protein trafficking in organisms with complex plastids supports this scenario (Cavalier-Smith, 1999, 2002; McFadden, 1999). Although McFadden postulated that the similar trafficking systems arose from convergent evolution, similarities can be explained more parsimoniously by a single endosymbiotic event with subsequent modification, than to argue convergent development of the system in multiple descendent lines. Furthermore, the early establishment of a protein trafficking system would "set the stage" for plastid re-gain in lineages that did not retain the original photosymbiont.
Cavalier-Smith (1999) proposes that the membrane fusion that placed the chloroplast within the lumen of the endoplasmic reticulum (ER) in cryptomonads, haptophytes and photosynthetic stramenopiles occurred in the ancestor of these taxa after the divergence from the ancestor of the alveolates. Our results do not support this scenario since the cryptomonads, whose plastids lie in the ER lumen, emerge prior to the divergences of the alveolates (van den Hoek et al., 1995) (see Fig. 6). However, our results are consistent with the proposal that the dinoflagellates with peridinin containing plastids, which are basal among photosynthetic dinoflagellates, have tertiary plastids. Early placement of the photobiont within the ER would have allowed a simple direct protein import pathway to develop during the initial stabilization of the endosymbiont in a secondary symbiogenesis.
Furthermore, the chromalveolate theory does not account for the alveolate plastid being located in a compartment other than the ER and trafficking proteins to the plastid via the secretory pathway (Schwartzach et al., 1998; Waller et al., 2000). Optimization indicates that the ancestors at nodes marking the divergence of kathablepharids and alveolates possessed "conoids." If the original secondary chlorophyll-c-containing plastid was lost deep within the alveolate clade and subsequently the ancestor of the peridinin-containing dinoflagellates obtained a replacement plastid via myzo- or phagocytosis of another chlorophyll-c-containing photobiont, descendents of this organism would have tertiary plastids appearing to be related to the original secondary chlorophyll-c-containing plastid (Fig. 6). This proposal is congruent with an extensive alveolate SSU rRNA tree (Saldarriaga et al., 2001), the similarity in chlorophyll c content between cryptomonads and dinoflagellates (van den Hoek et al., 1995), the close relationship of GAPDH genes of dinoflagellates and plastid targeted GAPDH genes of cryptomonads (Fagan et al., 1998; Fast et al., 2001), and the proposal that all peridinin- and fucoxanthin-containing dinoflagellates possess plastids that are tertiary (Yoon et al., 2002). Although the closer relationship between cryptomonads and heterokonts than between haptophytes and heterokonts based on rbcL gene sequences has prompted the proposal that haptophytes acquired a red type plastid convergently (Daugbjerg and Andersen, 1997a, b), that study de-emphasized the strong support shown for a clade with secondary chlorophyll-c-containing plastids that includes the haptophytes, analyzed only a single gene, and failed to account for similarities in plastid pigmentation and morphology between haptophytes and heterokonts.
Metazoan history may have also included the acquisition of a primary photoendosymbiont. If the glaucophytes, which in molecular analyses sometimes are positioned close to the cryptophytes (Bhattacharya et al., 1995; Fraunholz et al., 1997; Cavalier-Smith, 2000b, 2002; Kühn et al., 2000), arose prior to the divergence of the red and green algae and green plants, the uptake of a cyanobacterium by a excavate-like ancestor would have been part of the history of virtually all living eukaryotes including the metazoans. Moreover, the presence of the genes for 6-phosphogluconate dehyrogenase (gnd) of cyanobacterial origin in a heterolobosean point to a basal acquisition of a primary plastid (Andersson and Roger, 2002).
The results presented here, although preliminary, seem to contradict the idea that metazoans arose directly from basal taxa either in an explosive radiation of virtually all eukaryotes or in an early bipartion that isolated the opisthokonts from other eukaryotes (Cavalier-Smith, 2002). On the contrary our results seem to suggest that the metazoans shared a complex evolutionary history with many other eukaryote taxa (Figs. 3, 5, 7). The ground patterns inferred for the common ancestors of higher taxa including the metazoans can reveal critical steps in the acquisition of genomic and morphological complexity (Figs. 5, 7). Features acquired in these stem groups would have greatly influenced the evolution of the metazoans. These characters include a) an armor of scales, first organic and on both flagella and cell body and later siliceous and only on the cell body, b) primary (?) and secondary endophotosymbionts; the secondary would have been a eukaryote with a plastid of red algal origin conveying both nuclear and plastid genes to the ancestral genome, c) a conoid feeding apparatus in a auto/heterotroph that was perhaps predatory, d) complex transformations in body plans during their life cycle, including amoeboid or even centroheliozoan stages, and e) social behavior that may be linked to the rapid development of multicellularity and the differentiation of a multitude of cell types.
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This study also challenges other preconceptions regarding the evolution of eukaryotes. The sister relationship between the clade containing ramicristates and opistokonts (hence metazoans) and that of stramenopiles contradicts molecular analyses that usually align the alveolates with stramenopiles (Saunders et al., 1995
; Germot and Philippe, 1999; Baldauf et al., 2000; Cavalier-Smith, 2000a; but also see Van de Peer et al., 2000; Lopez-Garcia et al., 2001; Moon van der Staay et al., 2001). In addition, many key eukaryote apomorphies appear to represent paraphyletic grades of organization. Not only is the alveolar membrane system, the defining apomorphy of the "alveolates," found outside that group, the conoid, which is generally thought to be to be restricted to perkinsids and the apicomplexan, may be homologous sensu lato to conoid-like structures in ciliophorans, kathablepharids, the dinoflagellates, and perhaps haptophytes and certain cercozoans. The ability of characters to evolve and undergo complex transformations is not fully appreciated by evolutionary biologists. Character states must be analyzed in depth because they may define paraphyletic grades rather than monophyletic clades. Complexity, even that which was acquired at the unicellular level, would have impacted the mode and tempo of the metazoan radiation in the Late Neoproterozoic and Lower Cambrian. The morphology of the immediate ancestor of the metazoans may have been deceptively simple, a paltry reflection of the genomic complexity that could have accumulated over a long evolutionary history shared with numerous other eukaryote groups. If such stored complexity were unmasked with the development of a type of multicellularity in which there were no cell walls to interfere with interactions among cells, it could have influenced dramatically the scope and timing of the diversification that followed. Thus any discussion of the metazoan radiation needs to include the history of other eukaryote groups. The most basic attributes of eukaryotes other than metazoans, and perhaps plants and fungi, are poorly understood, and the resulting gaps in our knowledge are a serious impediment to understanding pivotal events in the origin and early evolution of the Metazoa.
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ACKNOWLEDGMENTS |
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The authors gratefully acknowledge students of our graduate seminar course, Cells, Organisms, and Evolution who delved deeply into the mysteries of the eukaryotes and thank especially Claire Bird and Beth Hudson for their insights and efforts in mining the literature. We also thank the Department of Biology, Graduate Studies and Research, and the College of Arts and Sciences for financial support. This symposium was supported by the National Science Foundation under Grant No. 0130902 (to Ruth Ann Dewel, Mark Martindale, and Dan McShea).
Note Added in Proof
A significant study (Yoon, H. S., J. D. Hackett, G. Pinto, and D. Bhattacharya. 2002. The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. U.S.A. 99:15507–15512) supporting a single secondary origin of a chlorophyll-c-containing plastid has appeared since this paper went to press.
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FOOTNOTES |
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1 From the Symposium New Perspectives on the Origin of Metazoan Complexity presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: dewelra{at}appstate.edu
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