Evolutionary ecology of colonial reef-organisms, with particular reference to corals

Sedentary reef-organisms such as sponges, colonial coelenterates, bryozoans and compound ascidians produce repeated modules (aquiferous systems, polyps, zooids) as they grow. Modular construction alleviates constraints on biomass imposed by mechanical and energetic factors that are functions of the surface area to volume ratio. Colonies thus may grow large whilst preserving optimal modular dimensions. Among corals, optimal polyp size is smaller in the more autotrophic than in the more heterotrophic species. Modular construction allows flexibility of growth form, which can adapt to factors such as water currents, silting, light intensity and proximity of competitors. Modular colonies have great regenerative capacities, even separated fragments may survive and grow into new colonies. All fragments from a parental colony are genetically identical and large branching corals frequently undergo clonal propagation through fragmentation during storms. Soft corals can also fragment endogenously. By spreading the risk of mortality among independent units, the generation and dispersal of fragments lessens the likelihood of clonal extinction. In spite of their ability to propagate asexually, most benthic colonial animals also reproduce asexually. The selective advantages of the genetic diversity among sexually produced offspring seem not to be linked with dispersal, but probably lie in the biological interactions with competitors, predators and pathogens in the parental habitat. Age at first sexual maturity and the proportional investment of resources in sexual reproduction are related to colonial survivorship. Small branching corals on reef flats grow quickly, attain sexual maturity within 1–4 years, planulate extensively, but reach only small sizes before dying. Massive corals are longer lived and have the opposite characteristics of growth and reproduction. Most sessile reef organisms compete for space, food or light. Faster growers can potentially outcompete slower growers, but are often prevented from doing so by several forms of aggression from competitors and by the damage inflicted by storms. Competitive interactions among sedentary organisms on coral reefs are unlikely to be linear or deterministic, and so the co-existence of diverse species is possible.     

On the mechanism of the modular primer effect.

Modular primers are strings of three contiguously annealed unligated oligonucleotides (modules) as short as 5- or 6-mers, selected from a presynthesized library. It was previously found that such strings can prime DNA sequencing reactions specifically, thus eliminating the need for the primer synthesis step in DNA sequencing by primer walking. It has remained largely a mystery why modular primers prime uniquely, while a single module, used alone in the same conditions, often shows alternative priming of comparable strength. In a puzzling way, the single module, even in a large excess over the template, no longer primes at the alternative sites, when modules with which it can form a contiguous string are also present. Here we describe experiments indicating that this phenomenon cannot be explained by cooperative annealing of the modules to the template. Instead, the mechanism seems to involve competition between different primers for the available polymerase. In this competition, the polymerase is preferentially engaged by longer primers, whether modular or conventional, at the expense of shorter primers, even though the latter can otherwise prime with similar or occasionally higher efficiency.     

Spatial interactions within modular organisms: genetic heterogeneity and organism fitness

Modular organisms are composed of iterated units of construction that vary in their spatial arrangement. This variation is expected to affect the fitness of modular organisms due to interactions among neighboring modules and the potential for such organisms to be genetically heterogeneous. We devise a spatially explicit model to investigate how spatial interactions among neighboring modules affect organism fitness. We show that fitness is strongly dependent on the spatial arrangement of modules in both genetically homogeneous and heterogeneous organisms, and that the magnitude of the variation is dependent on the strength of interactions among modules. Organism fitness is more variable with interactions among modules that are symmetrical (each affects each other in the same directions) than with asymmetrical interactions (neighbors affect each other in different directions). We conclude by discussing potential extension of the present framework to a general dynamic model of spatially structured organism development.     

SEASONAL MODULE DYNAMICS OF TURBINARIA TRIQUETRA (FUCALES,PHAEOPHYCEAE) IN THE SOUTHERN RED SEA1

Module dynamics in the fucoid alga Turbinaria triquetra (J. Agardh) Kützing were studied on a shallow reef flat in the southern Red Sea. Seasonal patterns in thallus density and size were determined, and the initiation, growth, reproduction, and shedding of modules were studied using a tagging approach. The effects of module density and module/thallus size on module initiation, growth, reproduction, and shedding were analyzed, and the occurrence of intraspecific competition among modules was examined. Seasonal variation occurred mainly at the modular level. There was a restricted period of new module formation in the cooler season, followed by fast growth and reproduction, massive shedding of modules from the end of the cooler season onward, and strongly reduced biomass in summer. There was no evidence of suppressed growth in small modules due to intraspecific competition. Module density and thallus/module size had opposite effects on elongation rates. High module densities enhanced maximum elongation rates (fastest‐growing module per thallus), resulting in longer thalli. On the other hand, elongation rates decreased and tissue loss increased with increasing module length. Reproduction had no clear effect on elongation rates, indicating that there was no direct trade‐off between reproduction and growth. The apparent size‐dependence of reproduction was due to delayed fertility in young modules. Module initiation and shedding were independent of module density. Shedding was also independent of module size and reproductive status. We conclude that seasonal changes in the environment affect module initiation, growth, reproduction, and shedding, whereas density and size‐dependent processes mainly affect growth rates.     

What does it take to evolve behaviorally complex organisms?

What genotypic features explain the evolvability of organisms that have to accomplish many different tasks? The genotype of behaviorally complex organisms may be more likely to encode modular neural architectures because neural modules dedicated to distinct tasks avoid neural interference, i.e. the arrival of conflicting messages for changing the value of connection weights during learning. However, if the connection weights for the various modules are genetically inherited, this raises the problem of genetic linkage: favorable mutations may fall on one portion of the genotype encoding one neural module and unfavorable mutations on another portion encoding another module. We show that this can prevent the genotype from reaching an adaptive optimum. This effect is different from other linkage effects described in the literature and we argue that it represents a new class of genetic constraints. Using simulations we show that sexual reproduction can alleviate the problem of genetic linkage by recombining separate modules all of which incorporate either favorable or unfavorable mutations. We speculate that this effect may contribute to the taxonomic prevalence of sexual reproduction among higher organisms. In addition to sexual recombination, the problem of genetic linkage for behaviorally complex organisms may be mitigated by entrusting evolution with the task of finding appropriate modular architectures and learning with the task of finding the appropriate connection weights for these architectures.     

A general model for selection among modules in haplo-diploid life histories

Genetic variation resulting from changes during somatic development in modular organisms may be inherited by subsequent generations due to the late development of their germ line. As a consequence, both sexually and asexually produced offspring may be genetically variable. The presence of heritable intraclonal variation and the great life history variation among modular organisms requires that evolutionary theory does not limit selection to only that occurring among individuals resulting from meiosis and zygote formation. To allow for variation within clonal lineages, and encompass a wide variety of life histories, we construct a simple model of selection among modules in life histories that contain both haploid and diploid phases, such as that seen among many multicellular algae. Selection among modules is a demographic process with module performance depending on its genotype at a single locus with two alleles. The model is used to simulate the spread of a beneficial allele in life histories that vary in the relative amount of sexual and asexual reproduction. The time taken for allele fixation is shown to depend on both demographic and genetic factors.     

SEASONAL MODULE DYNAMICS IN SARGASSUM SUBREPANDUM (FUCALES,PHAEOPHYTA)1

Module dynamics of the fucoid alga SARGASSUM SUBREPANDUM (Forssk.) C. Agardh was studied in the southern Red Sea. Seasonal variation in thallus density and size was determined, and the initiation, growth, reproduction, and shedding of modules (primary laterals) were ascertained, using a tagging approach. Possible effects of different size‐related parameters on module initiation, growth, reproduction, and shedding were analyzed in the context of contradicting results for other macroalgae, in comparison with terrestrial plants. Thallus density varied little; most of the seasonal variation occurred at the modular level. A restricted period of new module formation early in the cooler season was followed by fast growth and reproduction. Massive shedding of modules occurred toward the end of the cooler season leading to strongly reduced biomass in summer. There was some evidence that high module numbers inhibited new module formation and enhanced the maximum module elongation rate (fastest‐growing module per thallus). On the other hand, elongation rates generally decreased, and apical tissue losses increased with increasing module length. This response was observed over a wide size range, suggesting grazing losses. There was no evidence of suppressed growth in small modules due to intraspecific competition. Elongation rates remained unaffected by reproductive status, indicating that there was no direct trade‐off between growth and reproduction. Module survivorship was independent of module number and size, but fertile modules were more persistent than vegetative ones. We conclude that module dynamics are determined by seasonal changes in the environment, size‐dependent processes, and interactions among the modules.     

On the Classification and Evolution of Protein Modules

Our efforts to classify the functional units of many proteins, the modules, are reviewed. The data from the sequencing projects for various model organisms are extremely helpful in deducing the evolution of proteins and modules. For example, a dramatic increase of modular proteins can be observed from yeast to C. elegans in accordance with new protein functions that had to be introduced in multicellular organisms. Our sequence characterization of modules relies on sensitive similarity search algorithms and the collection of multiple sequence alignments for each module. To trace the evolution of modules and to further automate the classification, we have developed a sequence and a module alerting system that checks newly arriving sequence data for the presence of already classified modules. Using these systems, we were able to identify an unexpected similarity between extracellular C1Q modules with bacterial proteins.     

When can a clonal organism escape senescence?

Abstract Some clonal organisms may live for thousands of years and show no signs of senescence, while others consistently die after finite life spans. Using two models, we examined how stage-specific life-history rates of a clone's modules determine whether a genetic individual escapes senescence by replacing old modules with new ones. When the rates of clonal or sexual reproduction and survival of individual modules decline with age, clones are more likely to experience senescence. In addition, the models predict that there is a greater tendency to find senescence in terms of a decline in the rate of sexual reproduction with clone age than in terms of an increase in the probability of clone mortality, unless rates of sexual reproduction increase dramatically with module stage. Using a matrix model modified to represent the clonal lifestyle, we show how a trade-off between sexual and clonal reproduction could result in selection for or against clonal senescence. We also show that, in contrast to unitary organisms, the strength of selection on life-history traits can increase with the age of a clone even in a growing population, countering the evolution of senescence.     

Morphological integration and serial homology: A case study of the cranium and anterior vertebrae in salamanders

Serial homology or the repetition of equivalent developmental units and their derivatives is a phenomenon encountered in a variety of organisms, with the vertebrate axial skeleton as one of the most notable examples. Serially homologous structures can be viewed as an appropriate model system for studying morphological integration and modularity, due to the strong impact of development on their covariation. Here, we explored the pattern of morphological integration of the cranium and the first three serially homologous structures (atlas, first, and second trunk vertebrae) in salamandrid salamanders, using micro-CT scanning and three-dimensional geometric morphometrics. We explored the integration between structures at static and evolutionary levels. Effects of allometry on patterns of modularity were also taken into account. At the static level (within species), we analyzed inter-individual variation in shape to detect functional modules and intra-individual variation to detect developmental modules. Significant integration (based on inter-individual variation) among all structures was detected and allometry is shown to be an important integrating factor. The pattern of intra-individual, asymmetric variation indicates statistically significant developmental integration between the cranium and the atlas and between the first two trunk vertebrae. At the evolutionary level (among species), the cranium, atlas, and trunk vertebrae separate as different modules. Our results show that morphological integration at the evolutionary level coincides with morphological and functional differentiation of the axial skeleton, allowing the more or less independent evolutionary changes of the cranial skeleton and the vertebral column, regardless of the relatively strong integration at the static level. The observed patterns of morphological integration differ across levels, indicating different impacts of developmental and phylogenetic constraints and functional demands.     

Characterization and Comparison of the Tissue-Related Modules in Human and Mouse

Background

Due to the advances of high throughput technology and data-collection approaches, we are now in an unprecedented position to understand the evolution of organisms. Great efforts have characterized many individual genes responsible for the interspecies divergence, yet little is known about the genome-wide divergence at a higher level. Modules, serving as the building blocks and operational units of biological systems, provide more information than individual genes. Hence, the comparative analysis between species at the module level would shed more light on the mechanisms underlying the evolution of organisms than the traditional comparative genomics approaches.

Results

We systematically identified the tissue-related modules using the iterative signature algorithm (ISA), and we detected 52 and 65 modules in the human and mouse genomes, respectively. The gene expression patterns indicate that all of these predicted modules have a high possibility of serving as real biological modules. In addition, we defined a novel quantity, “total constraint intensity,” a proxy of multiple constraints (of co-regulated genes and tissues where the co-regulation occurs) on the evolution of genes in module context. We demonstrate that the evolutionary rate of a gene is negatively correlated with its total constraint intensity. Furthermore, there are modules coding the same essential biological processes, while their gene contents have diverged extensively between human and mouse.

Conclusions

Our results suggest that unlike the composition of module, which exhibits a great difference between human and mouse, the functional organization of the corresponding modules may evolve in a more conservative manner. Most importantly, our findings imply that similar biological processes can be carried out by different sets of genes from human and mouse, therefore, the functional data of individual genes from mouse may not apply to human in certain occasions.     

Invariant Features of Memory Capacity

Our purpose in these experiments was to study short-term (immediate) and long-term memory in the memorization of the same subject matter. By memory capacity is meant the number of units a person is able to reproduce in one repetition, or on an average in one repetition. In short-term reception and full reproduction of the material to be memorized, short-term memory capacity is commensurate with the number of units reproduced. Long-term memory capacity reflects the ability to accumulate as well as to retain information. When the material to be remembered exceeds the short-term memory capacity, the first reproduction is incomplete, and multiple presentation and repetition of the information are necessary for error-free and complete reproduction. In this case the memory capacity is equal to the number of units contained in the presented material divided by the number of repetitions.     

From asexual to eusocial reproduction by multilevel selection by density-dependent competitive interactions

A game theoretical model is developed to illustrate that multilevel selection by density-dependent competitive interactions in mobile organisms might have played a major role in the evolutionary transitions from asexual over sexual to eusocial reproduction. The model has four equilibria with selection occurring among interacting units of respectively one, two, three, and up to infinitely many individuals. The different equilibria are characterised by different levels of competitive interactions among interacting units, and these levels select for different levels of sexual and co-operative reproduction among the individuals of the units. The model predicts: (i) that low-energy organisms with negligible body masses have asexual reproduction; (ii) that high-energy organisms with non-negligible body masses in evolutionary equilibria have sexual reproduction between a female and a male; (iii) that high-energy organisms with non-negligible body masses that increase exponentially at an evolutionary steady state have co-operative reproduction between a sexual pair and a single sexually produced offspring; and (iv) that high-energy organisms with upward constrained body masses have eusocial reproduction between a sexual pair and up to an infinite number of sexually produced offspring workers.     

Modularity and the units of evolution

Summary While many developmental processes (e. g., gene networks or signaling pathways) are astonishingly conserved during evolution, they may be employed differently in different metazoan taxa or may be used multiply in different contexts of development. This suggests that these processes belong to building blocks or modules, viz., highly integrated parts of the organism, which develop and/or function relatively independent from other parts. Such modules may be relatively easy to dissociate from other modules and, therefore, could also serve as units of evolution. However, in order to further explore the implications of modularity for evolution, the vague notion of “modularity” as well as its relation to concepts like “unit of evolution” need to be more precisely specified. Here, a module is characterized as a certain type of dynamic pattern of couplings among the constituents of a process. It may or may not form a spatially contiguous unit. A unit of selection is defined as a unit of those constituents of a reproducing process/system, which exists in different variants and acts as a non-decomposable unit of fitness and variant reproduction during a particular selection process. The more general notion of a unit of evolution is characterized as a nondecomposable unit of constituents with reciprocal fitness dependence, be it due to fitness epistasis or due to the lack of independent variability. Because such fitness dependence may only be observed for some combinations of variants, several constituents may act as a unit of evolution only with a certain probability (coevolution probability). It is argued, that under certain conditions modules are likely to act as units of evolution with high coevolution probabilities, because there is likely to be a close tie between the pattern of couplings of the constituents of a reproducing system and their interdependent fitness contributions. Moreover and contrary to the traditional dichotomy of genes versus organisms as units of selection, modules tend to be more important in delimiting actual units of selection than either organisms or genes, because they are less easily disrupted by recombination than organisms, while having less contextsensitive fitness values than genes. Finally, it is suggested that the evolution of modularity is self-reinforcing, because the flexibility of intermodular connections facilitates the recombination among modules and their multiple employment in new contexts.     

Autonomous replication in human cells of multimers of specific human and bacterial DNA sequences.

Using modules of a specific 2,712-bp human DNA sequence and a specific 2,557-bp Escherichia coli DNA sequence, we created plasmids containing between 1 and 12 modules of single or chimeric sequence composition and tested them in human cells for their autonomous replication ability. We found that replication efficiency per generation increased with successive addition of human modules, to essentially 100% by six copies. Although a single copy of the bacterial module had negligible replication ability, the replication efficiency per generation of 12 bacterial modules was 66%. Chimeras composed of human and bacterial modules displayed intermediate replication levels. We also used two-dimensional gel electrophoresis to physically map where replication initiated on a half human-half E. coli plasmid. Our results suggest that autonomous replication in human cells is stimulated by simple sequence features which occur frequently in human DNA but are more rare in bacterial DNA.     

MAP kinases: universal multi-purpose signaling tools

MAP (mitogen-activated protein) kinases are serine/threonine protein kinases and mediate intracellular phosphorylation events linking various extracellular signals to different cellular targets. MAP kinase, MAP kinase kinase and MAP kinase kinase kinase are functional protein kinase units that are conserved in several signal transduction pathways in animals and yeasts. Isolation of all three components was also shown in plants and suggests conservation of a protein kinase module in all eukaryotic cells. In plants, MAP kinase modules appear to be involved in ethylene signaling and auxin-induced cell proliferation. Therefore, coupling of different extracellular signals to different physiological responses is mediated by MAP kinase cascades and appears to have evolved from a single prototypical protein kinase module which has been adapted to the specific requirements of different organisms.     

Geometrical model of spiral-cyclical self-organization of morphofunctional modules with two-dimensional (2D) transfer channels

The general model of spiral-cyclic self-organization of morphofunctional modules has been studied with the help of elliptic Riemannian geometry. Depending on the level of hierarchy cells, groups of cells, macromolecules or subcellular components can function as separate biological units. The hierarchically coordinated morphofunctional modules of biological pattern with two-dimensional (2D) channels of morphogenes transfer are formed in the process of geometric transformation. The width of 2D channel is regulated by module parameters, whereas the direction of transport is controlled by vector of module electrostatic field. The disturbance of morphogenesis in the model is regarded as a change of reciprocal hierarchically coordinated arrangement of morphofunctional modules that causes branching of 2D channels without general power- and mass transfer. The model can be used for constructing concrete analogies of self-organization of morphofunctional modules in onto- and phylogenesis.     

Life in the colonies: learning the alien ways of colonial organisms

Who needs to go to outer space to study alien beings when the oceans of our own planet abound with bizarre and unknown creatures? Many of them belong to sessile clonal and colonial groups, including sponges, hydroids, corals, octocorals, ascidians, bryozoans, and some polychaetes. Their life histories, in many ways unlike our own, are a challenge for biologists. Studying their ecology, behavior, and taxonomy means trying to “think like a colony” to understand the factors important in their lives. Until the 1980s, most marine ecologists ignored these difficult modular organisms. Plant ecologists showed them ways to deal with the two levels of asexually produced modules and genetic individuals, leading to a surge in research on the ecology of clonal and colonial marine invertebrates. Bryozoans make excellent model colonial animals. Their life histories range from ephemeral to perennial. Aspects of their lives such as growth, reproduction, partial mortality due to predation or fouling, and the behavior of both autozooids and polymorphs can be studied at the level of the colony, as well as that of the individual module, in living colonies and over time.     

Localization of hydrogen-bonds within modules in barnase

Proteins in eukaryotes are composed of structural units, each encoded by discrete exons. The protein module is one such structural unit; it has been defined as the least extended or the most compact contiguous segment in a globular domain. To elucidate roles of modules in protein evolution and folding, we examined roles of hydrogen bonds and hydrophobic cores, as related to the stability of these modules. For this purpose we studied barnase, a bacterial Rnase from Bacillus amylolique-faciens. Barnase is decomposed into at least six modules, M1–M6; the module boundaries are identified at amino acid residues 24, 52, 73, 88, and 98. Hydrogen bonds are localized mainly within each of the modules, with only a few between them, thereby indicating that their locations are designed to primarily stabilize each individual module. To obtain support for this notion, an analysis was made of hypothetical modules defined as segments starting at a center of one module and ending at the center of the following one. We found that the hydrogen bonds did not localize in each hypothetical module and that many formed between the hypothetical modules. The native conformations of modules of barnase may be specified predominantly by interactions within the modules. © 1993 Wiley-Liss, Inc.