The Society for Integrative and Comparative Biology
Fission in Sea Anemones: Integrative Studies of Life Cycle Evolution1
1 Moss Landing Marine Laboratories, California State University, 8272 Moss Landing Road, Moss Landing, California 95039
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Sea anemones (Phylum Cnidaria; Class Anthozoa, Order Actiniaria) exhibit a diversity of developmental patterns that include cloning by fission. Because natural histories of clonal and aclonal sea anemones are quite different, the gain and loss of fission is an important feature of actiniarian lineages. We have used mitochondrial DNA and nuclear intron DNA phylogenies to investigate the evolution of longitudinal fission in sixteen species in the genus Anthopleura, and reconstructed an aclonal ancestor that has given rise at least four times to clonal descendents. For A. elegantissima from the northeastern Pacific Ocean, a transition to clonality by fission was associated with an up-shore habitat shift, supporting prior hypotheses that clonal growth is an adaptation to the upper shore. Fission in Actiniaria likely precedes its advent in Anthopleura, and its repeated loss and gain is perplexing. Field studies of the acontiate sea anemone Aiptasia californica provided insight to the mechanisms that regulate fission: subtidal Aiptasia responded to experimentally destabilized substrata by increasing rates of pedal laceration. We put forth a general hypothesis for actiniarian fission in which sustained tissue stretch (a consequence of substratum instability or intrinsic behavior) induces tissue degradation, which in turn induces regeneration. The gain and loss of fission in Anthopleura lineages may only require the gain and loss of some form of stretching behavior. In this view, tissue stretch initiates a cascade of developmental events without requiring complex gene regulatory linkages.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONTHE SEA ANEMONE GENUS...EVOLUTIONARY ORIGINS OF FISSION...EVOLUTION OF FISSION MECHANISMS...CONCLUDING REMARKSReferences |
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The simplicity of the cnidarian body plan stands in contrast to an astounding variety of complex modular morphologies and life cycles (Hyman [1940]
; Pearse [1987]; Brusca and Brusca [2003]; for beautifully illustrated anthozoan examples, see Veron and Stafford-Smith [2000]; Fabricius and Alderslade, [2001]). A generalized cnidarian body consists of a cylinder or dome with a marginal circle of tentacles surrounding a mouth, and is formed as either a polyp or a medusa (Hyman, 1940). However, considerable morphological complexity can be achieved by asexual production of additional polyps or medusae. When these asexual products remain interconnected, a colony is formed whose shape depends on their spatial arrangement (see Lasker and Sanchez [2004] for a recent review). Physical connection also provides the possibility of distributing functions, such as nutrient acquisition or reproduction, to different clonally produced polyps and medusae. This division of labor can lead to a high degree of polymorphism as exemplified by siphonophore hydrozoans (Totton and Bargmann, 1965) and pennatulacean anthozoans (Bayer, 1973). Clonally produced polyps or medusae need not remain interconnected, and fission (defined here as programmed physical separation) allows for further complexity of life cycles. A life cycle including both polypoid and medusoid phases that can be separate in space and scarcely overlapping in time characterizes many hydrozoans and most scyphozoans (overviews in Hyman, 1940; Pearse, 1987; Brusca and Brusca, 2003). Finally solitary polyps or medusae may clone to produce more of their kind. In short, different combinations of clonal growth, polymorphism, and fission together provide for the diversity of morphologies and life histories seen in the Cnidaria (Fig. 1). Because the developmental processes that lead to the observed diversity of forms and life cycles are probably relatively simple, cnidarians may be a useful group in which to study the interface of development, ecology, and evolution.
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aAnthozoan cnidarians lack the medusoid lifestage found in other Cnidaria. Anthozoan life cycles are therefore simpler and their evolution centers on the presence or absence of clonality and the development of polymorphism of polyps in colonial forms (Fig. 2). In the subclass Hexacorallia, polymorphism of polyps in colonies is unknown, so for this group, variation in life cycles simply involves fission. The presence or absence of fission in hexacoral life cycles is profoundly important for their ecology because colonies and solitary individuals interact with their environment very differently.
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In scleractinian corals, clonal growth occurs without fission and leads to colonies that can take on many morphologies that are determined by the spatial domain of polyp formation (Coates and Oliver, 1973
), with different morphologies adapted to different regimes of water movement and light (Done, 1983; Veron and Stafford-Smith, 2000; Pandolfi et al., 2002). In sea anemones (Order Actiniaria), clonal growth occurs with a variety of fission processes (Chia, 1976; Fautin, 1991) and leads to collections of individual polyps that may evolve social structure depending on the degree of interaction within and between clones (Francis, 1976; Purcell and Kitting, 1982; Ayre, 1987; Ayre and Grosberg, 1996).
Solitary polyps that never undergo fission are known for hard corals, sea anemones, and tube anemones (cerianthids), and these aclonal species can achieve very large body sizes which require mechanical and behavioral adaptations to water flow that are unnecessary for smaller polyps (Koehl, 1976; Sebens, 1976). We propose that fission in hexacorals can be tractably studied at molecular, cellular, ecological, and evolutionary levels, and this paper presents some of our recent work, mostly on members of the genus Anthopleura, to achieve this integrative understanding.
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THE SEA ANEMONE GENUS ANTHOPLEURA |
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SYNOPSISINTRODUCTIONTHE SEA ANEMONE GENUS...EVOLUTIONARY ORIGINS OF FISSION...EVOLUTION OF FISSION MECHANISMS...CONCLUDING REMARKSReferences |
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Anthopleura is a good model to investigate transitions between clonal and aclonal growth modes (Geller and Walton, 2001
). Several morphological traits characterize this genus of about 40 species, especially fighting pseudotentacles (acrorhagi) and adhesive warts (verrucae) on the body column (Carlgren, 1949; Daly, 2001, 2004). Although other genera of sea anemones have similar, apparently convergent structures, morphological and molecular phylogenetic investigations support the cohesiveness of the genus within the family Actiniidae, together with some members of the genus Bunodosoma (Geller and Walton, 2001; Daly, 2004).
Many species of Anthopleura are known to undergo longitudinal fission, which has been described in detail for A. nigrescens and A. elegantissima (Mathew, 1979; Sebens, 1983). Fission begins with the elongation of the animal along the biradial axis defined by the siphonoglyphs. The pedal disk takes the shape of the outline of an hour-glass, and tissue begins to separate at its constricted waist. This tissue rupture proceeds from the base toward the oral disk. Eventually, only the sphincter muscle that surrounds the oral disk connects the two halves of the dividing animal and this eventually breaks. In the laboratory, fission for A. elegantissima has taken 3–5 days (J.B.G., personal observation), although animals were collected after becoming elongated. Thus, the total period required for fission is not precisely known. Upon complete separation, the open edges of the body column quickly come into contact and heal. In the course of fission and healing, missing or damaged internal structures, such as mesenteries, stomodeum, and a siphonoglyph are regenerated.
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EVOLUTIONARY ORIGINS OF FISSION IN ANTHOPLEURA |
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A phylogeny of 13 species of Anthopleura revealed multiple origins of longitudinal fission in Anthopleura (Geller and Walton, 2001
). Here, we add three species to the phylogenetic analysis and adopt maximum likelihood methods to reanalyze the evolutionary history of fission (Pagel, 1997, 1999). The analysis reconstructs the ancestral growth mode of Anthopleura as solitary, with a minimum of four independent gains of clonality (Fig. 3).
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= 1.69) selected with the program Modeltest (Posada and Crandall, 1998Why has clonality arisen in each observed case? Francis (1979
, 1988) and Shick (1991) both noted the preponderance of fission, and longitudinal fission in particular, among sea anemones living in a high shore habitat. In a detailed discussion, (Francis, 1979) suggested that intensified competition favored clonal species which could preempt space quickly. Francis (1979) and Shick (1991) also suggested that aggregations of clonemates might resist harsh conditions in the upper intertidal zone better than solitary individuals by, for example, retaining water between individuals. Sebens (1979) analyzed body size in sea anemones in an energetic model, and interpreted clonal species as optimizing net energy gain in some food-size regimes by staying small. A more general energetic analysis would allow for variable potential for photosynthetic inputs, as zooxanthellae may provide considerable nutrition for many species of Anthopleura (Fitt et al., 1982; Shick and Dykens, 1984; Zamer and Shick, 1987; Davy et al., 1996; Verde and McCloskey, 1996; Müller-Parker and Davy, 2001). Species that lack zooxanthellae may be either solitary or clonal, and preliminary analyses did not show a phylogenetic correlation between growth mode and symbiosis (Geller, unpublished data). The implication of Sebens' (1979) study is that the high shore provides a food regime that favors small body size and a clonal growth mode. While the three proximate hypotheses (competition, stress, and energetics) differ, they are not mutually exclusive and all associate clonality with the high shore. Put as a broader phylogenetic hypothesis, clonality is predicted to evolve as species of Anthopleura invade the upper shore. This hypothesis can be tested by mapping the habitats used by each species onto a phylogenetic tree, inferring ancestral habitats, and testing for statistical association between habitat and life history shifts.
For northeastern Pacific species, phylogenetic analysis showed monophyly of three species: A. elegantissima, A. sola, and A. xanthogrammica (Geller and Walton, 2001). These three species are sympatric over much of their ranges, and A. elegantissima has an upper limit well above the other two (Hand, 1955; Morris et al., 1980; Ricketts et al., 1985; Pearse and Francis, 2000). This group can provide a limited test of the habitat shift hypothesis. Unfortunately, mitochondrial DNA in anthozoans evolves unusually slowly (Shearer et al., 2002) and our earlier data did not resolve the branching order in this group (Geller and Walton, 2001). For this reason, we explored the utility of nuclear intron sequences for resolving the relationships of closely related species (Fitzgerald and Geller, submitted). Phylogenetic trees constructed from an arginine kinase (AK) intron and a G-protein coupled receptor (GPCR) intron did not reveal monophyly of the three species, except for A. xanthogrammica in AK intron trees. However, both loci revealed three clades, each dominated by one species, and we interpret lack of monophyly as the persistence of ancestral polymorphism (Fig. 4). Therefore, we conclude that A. elegantissima and A. sola are sister species, and that A. xanthogrammica is the sister of those two. Molecular phylogenetics thus supports the prior conclusions based on the morphological similarity of A. elegantissima and A. sola (Hand, 1955; Pearse and Francis, 2000). By parsimony, we infer that clonality is a derived trait in A. elegantissima that evolved concurrently with or subsequent to a shift into the high shore habitat. The broader application of nuclear loci to other species and collection of more extensive distributional data will allow a fuller test of the phylogenetic hypothesis that clonality is an adaptation to the high shore in Anthopleura.
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EVOLUTION OF FISSION MECHANISMS IN ANTHOPLEURA |
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SYNOPSISINTRODUCTIONTHE SEA ANEMONE GENUS...EVOLUTIONARY ORIGINS OF FISSION...EVOLUTION OF FISSION MECHANISMS...CONCLUDING REMARKSReferences |
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The observation that clonality with fission has arisen several times in Anthopleura from a solitary ancestor leads to questions about the evolution of the mechanisms underlying fission. Before discussing this topic, it is worth pointing out again that clonality, with or without fission, is a pervasive aspect of cnidarian life cycles, and it is almost certain that fission was present in some ancestor of Anthopleura. Thus, while cloning by fission appears to have arisen independently in at least four instances in Anthopleura, it may be more accurate to consider these as the recurrence of clonality following its earlier loss. Fission is typical in many anthozoans as well as in Hydrozoa and Scyphozoa, so it is reasonable to hypothesize that the cellular and molecular mechanisms involved may be similar among all cnidarians. On the other hand, Dollo's Law states that the loss of complex characters is irreversible, and fission in Anthopleura (and, by extension, many other cnidarians) appears to contradict that notion if, indeed, fission is complex.
An understanding of fission at the cellular and molecular levels will help us explain why this particular character may be re-invented, while others are permanently lost (see Zufall and Rausher [2004] for a recent plant example). Unfortunately, although development of the cnidarian polyp has been extensively investigated (Galliot and Miller, 2000; Steele, 2002; Bode, 2003), the mechanisms by which fission is achieved have not been similarly studied. The clonal sea anemone Nematostella vectensis is small, transparent, and can easily be cultured (Hand and Uhlinger, 1992), and its genome sequence will soon be determined. Nematostella, therefore, may be the most promising cnidarian for investigation of the molecular basis of fission. However, Nematostella is a monotypic genus and therefore is not a great candidate for studying transitions in life history characters. In contrast, although limited as a laboratory model, Anthopleura is a large genus containing variation in life history and other ecologically relevant traits.
Two feasible approaches to study fission in Anthopleura are the exploration of candidate genes or a functional genomic approach. Candidate genes are those hypothesized to function in a particular process because of related activities in other contexts or organisms. If cloning by fission is viewed more generally as a form of tissue modeling seen in all metazoans, in which some cells proliferate and others die (Gilbert, 2000), knowledge from other organisms can suggest candidate genes. Conversely, given the basal position of cnidarians among metazoans, characterizing their tissue modeling genes may provide insight into the evolutionary origins of morphogenesis. Functional genomic approaches usually involve arraying complementary DNA (cDNA) probes and comparative hybridization of labeled messenger RNA to isolate those specifically associated with a process or phenotype. Candidate gene and array approaches are complementary, and expressed sequence tag (EST) projects that often precede array fabrication can yield candidates.
We isolated and sequenced 384 cDNA clones from a cDNA library constructed from tissue isolated from the region of fission in a dividing A. elegantissima. Recovered clones likely derive from abundant mRNAs based on the probability that a given message would be cloned and sequenced. Without comparison to other tissues or physiological states, shotgun sequencing from this cDNA library cannot be considered an analysis of differential gene expression during fission, but may nonetheless point to genes with involvement in this process. Sequences were compared to protein databases using the translated BLAST computer program (Altschul et al., 1990), and many of these have inferred functions that could be involved in fission (Table 1). Of particular interest are several with top matches with genes implicated in protein degradation (homologues of the metalloproteinases Podocoryne MP1 and Hydra MP2), tissue remodeling (homologue of human thrombospondin), cell signaling (homologues of Drosophila Notch, Delta, and Frizzled) and programmed cell death (homologues of human apoptosis inhibitor, and a human caspase recruitment domain). Thus, this preliminary survey of ESTs suggests a number of candidate genes. All BLAST results can be viewed at www.mlml.calstate.edu.
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Evolutionary reversibility of fission in Anthopleura
We return to the question of the evolutionary recurrence of fission in Anthopleura. As described earlier, fission is a sequence of events first observed as an elongation of the polyp followed by tissue separation and regeneration. As above, we are assuming that the genes involved in fission are conserved and are expressed in contexts other than fission. In this view, the difference between clonal and solitary species is that these genes in clonal species are coordinately regulated. The question of loss and gain of fission in Anthopleura is then one of the loss and gain of coordination of gene expression. A tenet of molecular evolution is that unused genes, broadly construed to include regulatory elements of DNA, mutate to disfunctionality over time (Li, 1997
; Brown, 2002). If this is so, the recurrent appearance of fission presents a conceptual difficulty–the gene coordination needed for fission should be easily lost in nascent aclonal species but regained rarely. However, just as the genes involved in fission likely have multiple contexts of expression, so might discrete developmental modules within the overall fission process. These processes are, broadly categorized, body elongation, tissue degradation, and regeneration. Viewed with time-lapse video, body elongation in Anthopleura elegantissima involves muscular activity similar to that in normal locomotion (J.B.G., personal observation). Regeneration that follows tissue degradation will occur after any injury, whether the source of the injury is extrinsic (e.g., from predators or mishap) or intrinsic (fission) (Mathew, 1979; Meszaros and Bigger, 1999). We suspect that the degradation and separation of tissues that occurs during fission involve developmental paths that function in morphogenesis. A central question is how these paths become linked in sequence? Our recent work on the environmental regulation of pedal laceration in Aiptasia leads us to hypothesize that stretching of tissue induces tissue degradation.
Tissue stretch and the induction of pedal laceration
Pedal laceration in sea anemones is a mode of fission which involves the spreading of the pedal disk and the degradation of tissue between the margin of the pedal disk and the body column. This produces crescent-shaped fragments which then regenerate into fully formed polyps. Anthony and Svane (1995) studied pedal laceration in Metridium senile growing on mussel shells. In laboratory studies, they found that anemones on live mussels had higher rates of laceration than those on dead shells, and they found that anemones on manually rotated mussel mimics had higher rates of laceration than those on unrotated mimics. This study implicated movement of the substratum as an environmental cue for pedal laceration.
We conducted related field studies on the sea anemone Aiptasia californica living on rhodoliths (spherical, unattached calcareous red alga) in Bahía Concepción, Baja California, Mexico (King, 2003). Rhodoliths occur in dense beds which cover subtidal sandy bottoms. Substratum movement was experimentally manipulated by manually stirring some patches, stabilizing others, and leaving some as unmanipulated controls. Like Anthony and Svane (1995), King (2003) found elevated rates of pedal laceration in stirred patches (Fig. 5). In a second experiment, sea anemones were recruited to plastic pipes that were then raised above the bottom. To expose them to a gentle form of substratum instability, some pipes were rotated 180° daily so that the top sides were moved to a downward position each 24 hr. Other pipes were not rotated. Anemones on rotated pipes had higher rates of pedal laceration (Fig. 6).
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These studies clearly implicate substratum movement as an inducer of pedal laceration, but do not point to the actual mechanism of induction. On live, motile mussels or stirred rhodoliths, pieces of the pedal disk of anemones might simply be torn. If so, the regulation of fission is purely environmental. However, anemones on mussel mimics or plastic pipes were subject only to a brief moment of rotation which presumably is no more stressful than ambient water flow. We hypothesize that movement of the substratum induces locomotion as the animal repositions itself with respect to water flow or light. If the trailing edge of the pedal disk lags behind the leading edge, the trailing margin of the pedal disk will be stretched. Stretch is known to induce programmed cell death in many tissues (e.g., Liu et al., 2002
; Sanchez-Esteban et al., 2002; Sotoudeh et al., 2002; Wernig et al., 2003; Hammerschmidt et al., 2004; Liao et al., 2004; Power et al., 2004). Most relevant, Mire (1998) and Mire and Venable (1999) found that when the sea anemone Diadumene (=Haliplanella) lineata was experimentally stretched, fission occurred with morphological evidence for apoptosis in the region of fission. We hypothesize that our results with Aiptasia are explained by "sticky locomotion" that results in tissue stretch, which in turns leads to programmed cell death and other tissue degrading processes, ultimately manifest as pedal laceration.
This view of pedal laceration in Aiptasia may give a clue to the evolution of longitudinal fission in distantly related Anthopleura and other sea anemones. The first step of longitudinal fission is the elongation of the body, causing the central tissues to experience stretch. This stretch may then induce programmed cell death, as suggested for Diadumene (Mire, 1998; Mire and Venable, 1999), and other tissue degrading processes. Once tissue loss occurs, regeneration would ensue as a direct consequence. The gain and loss of fission in Anthopleura therefore may require only the gain and loss of a behavior—longitudinal stretching. The behavior of longitudinal stretching must be induced by internal signals of body size or other intrinsic cues, and this signaling itself may be a complex phenomenon. However, the evolution of fission as a developmental feature could be rather simple.
Fission may be regulated by behaviors or environmental stresses that stretch tissue. Regeneration is a process that restores body patterning following fission, but such pattern formation does not require fission. In Anthopleura, budding of polyps from the body wall has been infrequently observed in species otherwise considered nonclonal (e.g., A. artemisia, J.B.G., personal observation). These observations imply that the genetic pathways required for clonality are retained in aclonal species, and that formation of a new polyp is not irrevocably linked to fission, as it appears to be in clonal sea anemones. Theoretically, the decoupling of fission and pattern formation could lead to the evolution of coloniality. Remarkably, this has now been discovered in the Actiniaria in Cereus herpetoides, in which polyps become elongated (as though preparing for longitudinal fission) and form additional mouths (Häussermann and Försterra, 2003). This is the only known incidence of coloniality in sea anemones but, as noted by Häusserman and Försterra (2003), this process resembles intratentacular budding in scleractinian corals. It appears possible that intratentacular budding may have arisen in phylogenetically distant taxa using very similar if not identical sets of genes and pathways.
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CONCLUDING REMARKS |
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SYNOPSISINTRODUCTIONTHE SEA ANEMONE GENUS...EVOLUTIONARY ORIGINS OF FISSION...EVOLUTION OF FISSION MECHANISMS...CONCLUDING REMARKSReferences |
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Clonality with or without fission is a pivotal developmental trait in the life cycle and ecology of many cnidarians, as well as other sessile invertebrates and plants. Its importance for demography (Jackson et al., 1985
; Harper et al., 1986; Karlson, 1999) has been extensively studied. The ecology and behavior of clonal invertebrates too has received much attention (Francis, 1973a, b, 1976, 1988; Buss, 1979; Jackson, 1979; Jackson et al., 1979; Ayre, 1983, 1987; Grosberg, 1988; Harvell and Grosberg, 1988; Buss, 1990; Ayre and Grosberg, 1995, 1996). Phylogenetic and paleontological studies have examined its evolutionary dynamic (Coates and Oliver, 1973; Jackson et al., 1985; Veron, 1995; Cheetham et al., 2001; Geller and Walton, 2001; McFadden et al., 2001). In cnidarians, the developmental biology of some aspects of clonality have been studied (Martinez et al., 1997; Cartwright et al., 1999; Cartwright and Buss, 1999). Given the successes of each of these approaches in isolation, cnidarian clonality is an outstanding model to integrate approaches for a more comprehensive, multilayered understanding at the interface of ecology, life history, and development.
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ACKNOWLEDGMENTS |
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Many thanks to Neil Blackstone for organizing this symposium and the invitation to participate. This work was supported by grants from the National Science Foundation (OCE9458350), the Dr. Earl and Ethyl Myers Oceanographic and Marine Biology Trust, the Lerner-Gray Fund for Marine Research, the Packard Foundation, and PADI Project Aware.
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FOOTNOTES |
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1 From the Symposium Model Systems for the Basal Metazoans: Cnidarians, Ctenophores, and Placozoans presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5– 9 January 2004, at New Orleans, Louisiana.
2 E-mail: geller{at}mlml.calstate.edu
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SYNOPSISINTRODUCTIONTHE SEA ANEMONE GENUS...EVOLUTIONARY ORIGINS OF FISSION...EVOLUTION OF FISSION MECHANISMS...CONCLUDING REMARKSReferences |
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