Integrative and Comparative Biology Advance Access originally published online on June 12, 2006
Integrative and Comparative Biology 2006 46(6):713-718; doi:10.1093/icb/icl009
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Applying the concept of metamorphosis to the crustose-to-erect thallus transition of macroalgae
* Center for Advanced Studies in Ecology and Biodiversity Santiago, Chile
Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile Santiago, Chile
Correspondence: 1E-mail: bsanteli{at}bio.puc.cl
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Synopsis |
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 Synopsis IntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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Metamorphosis is broadly defined as a more or less radical morphological change between 2 multicellular life stages within an organism's life phase, often marking the transition from pre-reproductive to reproductive stages. It involves structural reorganization and major physiological changes, generally under the control of endogenous and exogenous factors and often resulting in changes in habitat use. This concept has been applied to the crustose-to-erect thallus transition of some red algae and the present study evaluates the validity of such hypotheses. Available literature suggests that the crustose-to-erect thallus transition involves significant morphological and habitat changes, separating pre-reproductive and reproductive stages. The onset of the morphological changes (for example axis differentiation) appears regulated by endogenous signals (growth factors) and growth is modified by environmental factors. The algae do not exhibit structural reorganization, however, probably due to their simple morphological structure and the lack of several cell and tissue mechanisms involving cell motility. The presence of cell walls in the algae impairs cell motility and maintains the cell in a fixed position within the plant. These are important differences restricting the extension of the definition of metamorphosis to the crust-to-erect thallus transition. The above restrictions also seem to apply to other macroalgae, fungi, and terrestrial plants.
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Introduction |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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Life cycles and complex life-history transitions, including metamorphosis, often involve a large number of developmental processes that need to be accurately timed and coordinated with one another and with the environment (Heyland and others 2005
). Since such processes have evolved many times in different environments (Hadfield 2000), complex life-history transitions are popular areas of study to advance evolutionary biology through comparative studies of convergent developmental processes.
Complex life-history transitions occur in a high diversity of organisms and involve a wide variety of processes. Accordingly, their study has stimulated such a wide range of approaches, theories, and methods that at present it is difficult to summarize the knowledge in this area due to a lack of common grounds among the organisms and processes studied (Heyland and others 2006). Consequently, efforts are being made to find similarities in life-history transitions among different kinds of organisms to provide the frame for a more unified approach to the study of these processes. A unified approach hopefully will improve our present understanding of these transitions, eventually opening up new avenues of research.
Present efforts to unify the concept of metamorphosis comprise a search for similarities and convergences in life-history transitions among distantly related organisms. Traditionally restricted to the Animalia, the concept has recently been expanded (Bishop and Hodin 2001; Hodin 2006) to include life-stage transitions in other non-animal multicellular eukaryotes, such as the mycelium-to-fruiting body transitions of some fungi and the crustose-to-thallus transition of some red algae (Heyland and others 2005).
The adoption of common terms to describe transitions between vegetative and reproductive multicellular stages of life histories across distantly related organisms and different kingdoms would facilitate comparisons of equivalent morphological and physiological responses, molecular regulators and signaling systems. Before expanding the definition in search for similarities, however, some critical assessment seems necessary. Such an assessment should evaluate whether or not applying a concept based on organisms in one Kingdom to organisms from another Kingdom would violate biological constraints in the latter. Even though each Kingdom of organisms (sensu Whittaker 1969; Margulis 1971) may include several kinds of organisms (Santelices 1999), each Kingdom has basic biological properties (Buss 1982, 1987) that might restrict the general application of definitions and concepts across all of them. In the present study we evaluate this idea by applying the expanded concept of metamorphosis to the crustose-to-erect thallus transition of some red algal species. We start with a broad definition of metamorphosis. Then we evaluate the applicability of each component of this definition to the crustose-to-erect thallus transition. Finally, we discuss whether the concept could be applied to organisms from non-animal kingdoms.
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Definition of metamorphosis |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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Metamorphosis is understood (Hodin 2006
) as a more or less radical morphological change between 2 multicellular phases in an organism's life cycle, often marking the transition from a pre-reproductive to a reproductive life stage. It involves structural reorganization and major physiological and habitat changes and is controlled by endogenous and exogenous factors. |
The crustose-to-erect thallus transition in the red algae |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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Algal species in the Orders Corallinales, Hildenbrandiales, Palmariales, Gigartinales and Rhodymeniales all exhibit crustose-to-erect thallus transitions. After attachment, the spore divides by a wall perpendicular to the substratum. Several vertical and horizontal divisions follow, producing a hemispherical, polystromatic crust (Dixon 1973
; Gabrielson and Garbary 1986). Fifteen to thirty days after spore germination, one or a group of transversely dividing axial cells arise from within or from the surface of the crust, producing a number of axial filaments (Figs 1A and B). Axial filaments are often surrounded by lateral filaments that also exhibit apical divisions and increase the width of the emerging upright. The degree of aggregation between lateral and axial filaments varies among species, but in species with erect, foliose thalli there is a rather compact arrangement.
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The continued activity of axial and lateral apicals eventually leads to the formation of a macroscopically recognizable erect thallus arising from the crustose base (Fig. 1C). Thus, the crustose-to-erect thallus transition occurs during development of the gametophyte, the sporophyte, or both. The transition does not refer to interphase changes, for example from a crustose gametophyte to a foliose sporophyte, but it is restricted to intra-phase changes.
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Application of the conceptual components of metamorphic changes to the crustose-to-erect thallus transition of the red algae |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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Available literature is used to evaluate the application of the conceptual components of the above definition of metamorphosis to the crustose-to-erect thallus transition of the red algae (Table 1). All but one of the concepts are fulfilled by the algal life-stage transition.
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Within the morphological simplicity of the red algal thallus, the morphological changes involved in the emergence of the erect axes are significant. The process involves the differentiation of a number of axial cells that, by transverse divisions, produce filaments in a vertical direction, rising well above the level of the crust and originating a new erect axis. The net effect of this is a change in the direction of the main growth, from radial expansion of the crust to a vertical extension of the axis. In addition, the differentiation of axial and lateral filaments, both with apical initials, allows the increments in length and breadth of the erect axes.
The emergence and growth of the erect axis also implies a change of habitats. The growing thallus extends from the boundary layer and laminar sublayer habitats to places with higher water velocities, such as the turbulent sublayers (Neushul 1972; Charters and others 1973; Denny 1988; Lobban and Harrison 1994). It is generally known that water velocity modifies the net effects of several other abiotic factors on the growth of macroalgae (see review in Lobban and Harrison 1994), including irradiance, speed of nutrient exchange, sediment accumulation on the thallus, and epiphyte load. Therefore, even though the crustose-to-erect thallus transition in these red algal species does not involve a spatial shift, it does imply changes in the habitat conditions affecting the seaweed and changes in the physiological responses of the growing axes.
Evidence for endogenous and exogenous regulation of thallus uprising has been obtained, among others, through tissue cultures. The addition of different concentrations of several types of growth regulators to calluses of various algal species (see Table 2) results in a differentiation of apical initials and the growth of the erect axis. Studies on evolutionary patterns in auxin action (Cooke and others 2002) have concluded that the mechanisms mediating the responses of some of these hormones (for example indole-3-acetic acid) in land plants already existed in algae and bryophytes.
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The crustose-to-erect thallus transition can also be modified by environmental factors such as temperature, irradiance, and salinity. Although numerous studies (see Lobban and Harrison 1994
for review) have evaluated the effects of these factors on the growing axes under controlled laboratory conditions, only a few (for example Yokoya and others 1999) have worked with uprisings differentiated from calluses in tissue culture.
The crustose-to-erect thallus transition also separates pre-reproductive and post-reproductive stages in most of these algae. With a few exceptions (for example some species in the Corallinales), most taxa with erect axes generally differentiate reproductive structures only on those axes that, by later growth, become foliose, with morphologies ranging from cylindrical axes to expanded blades (see Wommersley 1996; Stegenga and others 1997 or Abbott 1999 for examples and descriptions).
Several organismic factors may also modify the number and timing of erect axis arising from basal crusts, especially among coalescing species. These include the number of spores coalescing during early recruitment (Santelices and others 1996, 1999) and the number of young recruits coalescing with older ones (Santelices and others 2004). Equivalent factors, however, have not been included in the definition of metamorphosis, probably because they do not occur or analogous responses are not found in metamorphic animals.
The crustose-to-thallus transition of the red algae does not involve structural remodeling as the metamorphic changes of animals do. Repeated observations of the uprising process (for example Fig. 1) only indicate cell and tissue proliferation, without evidence of cell or tissue transfers within the plant, as animals do during metamorphosis. Since this is the only component of metamorphic change not found in the algal life-stage transition under study, some evaluation of its importance seems necessary.
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Evaluation of differences |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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When exploring causes for the lack of structural remodeling in the life-stage transitions of the algae, 3 factors of general importance emerge. The first refers to the very simple body (thallus) structure of the algae, in comparison with animals. While in most animals, a diversity of tissues and specialized cells can be found, the crustose and erect axis of the algae have a relatively small variety of cells and tissues (cortex and medulla) conforming the structure of the growing axis.
A second important difference refers to the cellular and tissue mechanisms involved in metamorphosis in animals and their presence in macroalgae. While there are 6 potential processes in animals (Table 3), only cell and tissue proliferation are of common occurrence in macroalgae. At present, there is not enough information to know whether apoptosis occurs in red algae but it is clear that these organisms lack cell migration and tissue resorption. The presence of cell walls in algae impairs cell motility (Buss 1982, 1987), maintaining the cell in a fixed position within the plant. In turn, the lack of motility impairs cell migration and tissue resorption. In fact, macroalgae may move nutrients and organic substances from one part of the plant to another (see Lobban and Harrison 1994; Gonen and others 1996) but cannot reabsorb tissues. Cell fusions have been described in a few red macroalgal species during cystocarp formation (Gabrielson and Garbary 1986) or during spore coalescence (Santelices and others 1999) before cell walls are differentiated, but in general cell wall formation limits the capacity to fuse in these cells. Contiguous algal cells may establish cellular connections but they cannot fuse.
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The third general difference found between the metamorphic changes in most animals and the crustose-to-thallus transition of the red algae occurs at the individual level. During typical metamorphosis of animals, the whole individual of the previous metamorphic stage (for example a larva) transforms itself into the next metamorphic stage (for example a pupae). In contrast, in the crustose-to-erect thallus transition of the macroalgae, the crust (previous metamorphic stage) does not transform itself into the new, erect axis (new metamorphic stage). The crust remains there, normally growing radially and eventually originating additional erect axes. In this process the crustose-to-erect thallus transition of the red algae approaches the budding off medusae of scyphozoan and hydrozoan polyps rather than exhibiting a typical metamorphic transformation. A crustose-to-thallus transition also could be found in other types of macroalgae (for example Analipus, a brown alga) but it is expected that they exhibit the above differences described for the red algae. Similarly, several of the above differences probably occur also in fungi and land plants, the other examples of non-animal metamorphosis suggested (Bishop and Hodin 2001
; Heyland and others 2005), because these organisms also exhibit cell walls (Buss 1982, 1987). |
Conclusion |
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SynopsisIntroductionDefinition of metamorphosisThe crustose-to-erect thallus...Application of the conceptual...Evaluation of differencesConclusionReferences |
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It is concluded that the crustose-to-erect thallus transition of the red algae parallels many of the responses so far described for the metamorphic processes of Animalia. However, the algae exhibit important biological restrictions due to the presence of a cell wall, lack of cell motility, a very simple morphological structure, and the persistence of the later metamorphic stages after the emergence of the new metamorphic stage. Several of these constraints are also anticipated to occur in other kinds of macroalgae, fungi, and land plants.
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Acknowledgements |
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The authors express their gratitude to Dr J. Vial for discussions and ideas during the preparation of the study, to Dr F. Bozinovic for critical comments to early drafts of this manuscript, and to R. Finke for improving the grammar. This study was supported by grant FONDECYT 1060474, Chile. We are grateful to the Society for Integrative and Comparative Biology (SICB) for promoting and partially funding the Symposium "Metamorphosis: A multi-Kingdom approach." Furthermore we would like to thank the following organizations for their generous financial support: The University of Florida, the Whitney Laboratory for Marine Biosciences, the American Microscopical Society (AMS), and the SICB Division of Evolutionary Developmental Biology (DEDB).
Conflict of interest: None declared.
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Footnotes |
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From the symposium "Metamorphosis: A Multikingdom Approach" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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