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      Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae)

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      BMC Evolutionary Biology
      BioMed Central

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          Abstract

          Background

          Quantitative studies of the variation of disparity during ontogeny exhibited by the radiation of coral reef fishes are lacking. Such studies dealing with the variation of disparity, i.e. the diversity of organic form, over ontogeny could be a first step in detecting evolutionary mechanisms in these fishes. The damselfishes (Pomacentridae) have a bipartite life-cycle, as do the majority of demersal coral reef fishes. During their pelagic dispersion phase, all larvae feed on planktonic prey. On the other hand, juveniles and adults associated with the coral reef environment show a higher diversity of diets. Using geometric morphometrics, we study the ontogenetic dynamic of shape disparity of different head skeletal units (neurocranium, suspensorium and opercle, mandible and premaxilla) in this fish family. We expected that larvae of different species might be relatively similar in shapes. Alternatively, specialization may become notable even in the juvenile and adult phase.

          Results

          The disparity levels increase significantly throughout ontogeny for each skeletal unit. At settlement, all larval shapes are already species-specific. Damselfishes show high levels of ontogenetic allometry during their post-settlement growth. The divergence of allometric patterns largely explains the changes in patterns and levels of shape disparity over ontogeny. The rate of shape change and the length of ontogenetic trajectories seem to be less variable among species. We also show that the high levels of shape disparity at the adult stage are correlated to a higher level of ecological and functional diversity in this stage.

          Conclusion

          Diversification throughout ontogeny of damselfishes results from the interaction among several developmental novelties enhancing disparity. The bipartite life-cycle of damselfishes exemplifies a case where the variation of environmental factors, i.e. the transition from the more homogeneous oceanic environment to the coral reef offering a wide range of feeding habits, promotes increasing shape disparity of the head skeleton over the ontogeny of fishes.

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          Most cited references47

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          Heterochrony and allometry: the analysis of evolutionary change in ontogeny.

          The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.
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            Many-to-One Mapping of Form to Function: A General Principle in Organismal Design?

            We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R(2) = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.
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              DISPARITY: MORPHOLOGICAL PATTERN AND DEVELOPMENTAL CONTEXT

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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2011
                30 March 2011
                : 11
                : 82
                Affiliations
                [1 ]Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de Chimie (B6c), Université de Liège, B-4000 Liège, Belgium
                Article
                1471-2148-11-82
                10.1186/1471-2148-11-82
                3078888
                21450094
                10ed0945-2739-4535-8a92-7cf1368f7f53
                Copyright ©2011 Frédérich and Vandewalle; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 November 2010
                : 30 March 2011
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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