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      Paedomorphosis as an Evolutionary Driving Force: Insights from Deep-Sea Brittle Stars

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      Author(s): 1 , * , 2 , *
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      Journal: PLoS ONE
      Publisher: Public Library of Science

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          Abstract

          Heterochronic development has been proposed to have played an important role in the evolution of echinoderms. In the class Ophiuroidea, paedomorphosis (retention of juvenile characters into adulthood) has been documented in the families Ophiuridae and Ophiolepididae but not been investigated on a broader taxonomic scale. Historical errors, confusing juvenile stages with paedomorphic species, show the difficulties in correctly identifying the effects of heterochrony on development and evolution. This study presents a detailed analysis of 40 species with morphologies showing various degrees of juvenile appearance in late ontogeny. They are compared to a range of early ontogenetic stages from paedomorphic and non-paedomorphic species. Both quantitative and qualitative measurements are taken and analysed. The results suggest that strongly paedomorphic species are usually larger than other species at comparable developmental stage. The findings support recent notions of polyphyletic origin of the families Ophiuridae and Ophiolepididae. The importance of paedomorphosis and its correct recognition for the practice of taxonomy and phylogeny are emphasized.

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

          C P Klingenberg (1998)
          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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            Resynthesizing evolutionary and developmental biology.

            J Opitz, Jennifer A Raff, Jeffrey S. Gilbert (1996)
            A new and more robust evolutionary synthesis is emerging that attempts to explain macroevolution as well as microevolutionary events. This new synthesis emphasizes three morphological areas of biology that had been marginalized by the Modern Synthesis of genetics and evolution: embryology, macroevolution, and homology. The foundations for this new synthesis have been provided by new findings from developmental genetics and from the reinterpretation of the fossil record. In this nascent synthesis, macroevolutionary questions are not seen as being soluble by population genetics, and the developmental actions of genes involved with growth and cell specification are seen as being critical for the formation of higher taxa. In addition to discovering the remarkable homologies of homeobox genes and their domains of expression, developmental genetics has recently proposed homologies of process that supplement the older homologies of structure. Homologous developmental pathways, such those involving the wnt genes, are seen in numerous embryonic processes, and they are seen occurring in discrete regions, the morphogenetic fields. These fields (which exemplify the modular nature of developing embryos) are proposed to mediate between genotype and phenotype. Just as the cell (and not its genome) functions as the unit of organic structure and function, so the morphogenetic field (and not the genes or the cells) is seen as a major unit of ontogeny whose changes bring about changes in evolution.
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              Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships.

              John Wiens, Ronald Bonett, Paul Chippindale (2005)
              Evolutionary developmental biology ("evo-devo") has revolutionized evolutionary biology but has had relatively little impact on systematics. We show that similar large-scale developmental changes in distantly related lineages can dramatically mislead phylogenetic analyses based on morphological data. Salamanders are important model systems in many fields of biology and are of special interest in that many species are paedomorphic and thus never complete metamorphosis. A recent study of higher-level salamander phylogeny placed most paedomorphic families in a single clade based on morphological data. Here, we use new molecular and morphological data to show that this result most likely was caused by the misleading effects of paedomorphosis. We also provide a well-supported estimate of higher-level salamander relationships based on combined molecular and morphological data. Many authors have suggested that paedomorphosis may be problematic in studies of salamander phylogeny, but this hypothesis has never been tested with a rigorous phylogenetic analysis. We find that the misleading effects of paedomorphosis on phylogenetic analysis go beyond the sharing of homoplastic larval traits by paedomorphic adults, and the problem therefore is not solved by simply excluding suspected paedomorphic characters. Instead, two additional factors are critically important in causing paedomorphic species to be phylogenetically "misplaced": (1) the absence of clade-specific synapomorphies that develop during metamorphosis in nonpaedomorphic taxa and allow their "correct" placement and (2) parallel adaptive changes associated with the aquatic habitat of the larval stage. Our results suggest that the effects of paedomorphosis on phylogenetic analyses may be complex, difficult to detect, and can lead to results that are both wrong and statistically well supported by parsimony and Bayesian analyses.
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                Author and article information

                Contributors
                Michael Schubert: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 2 November 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 11
                Electronic Location Identifier: e0164562
                Affiliations
                [1 ]Swedish Museum of Natural History, Department of Zoology, Stockholm, Sweden
                [2 ]Zoological Museum, Moscow State University, Moscow, Russia
                Laboratoire de Biologie du Développement de Villefranche-sur-Mer, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: AM SS.

                • Formal analysis: AM SS.

                • Funding acquisition: AM SS.

                • Investigation: AM SS.

                • Methodology: AM SS.

                • Resources: AM SS.

                • Visualization: AM SS.

                • Writing – original draft: AM SS.

                • Writing – review & editing: AM SS.

                Article
                Publisher ID: PONE-D-16-16700
                DOI: 10.1371/journal.pone.0164562
                PMC ID: 5091845
                PubMed ID: 27806039
                SO-VID: 841898b6-349f-41d9-8a6b-db014e311126
                Copyright © © 2016 Stöhr, Martynov
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 25 April 2016
                Date accepted : 5 September 2016
                Page count
                Figures: 8, Tables: 4, Pages: 24
                Funding
                Funded by: Riksmusei vänner (supporters of the Swedish Museum of Natural History)
                Award Recipient :
                Funded by: Research project of MSU Zoological Museum
                Award ID: АААА-А16-116021660077-3
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100006769, Russian Science Foundation;
                Award ID: 14-50-00029
                Award Recipient :
                This work was supported by Riksmusei vänner (supporters of the Swedish Museum of Natural History; travel grant and extensive SEM), Research project of MSU Zoological Museum (AAAA-A16-116021660077-3) and by the Russian Science Foundation (grant 14-50-00029, morphological and SEM study, specimens deposition).
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Musculoskeletal System
                Subject: Spine
                Subject: Vertebrae
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Musculoskeletal System
                Subject: Spine
                Subject: Vertebrae
                Subject: Biology and Life Sciences
                Subject: Taxonomy
                Subject: Computer and Information Sciences
                Subject: Data Management
                Subject: Taxonomy
                Subject: Research and Analysis Methods
                Subject: Research Facilities
                Subject: Museum Collections
                Subject: Biology and Life Sciences
                Subject: Developmental Biology
                Subject: Morphogenesis
                Subject: Biology and Life Sciences
                Subject: Developmental Biology
                Subject: Evolutionary Developmental Biology
                Subject: Biology and Life Sciences
                Subject: Evolutionary Biology
                Subject: Evolutionary Developmental Biology
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Digestive System
                Subject: Teeth
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Digestive System
                Subject: Teeth
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Jaw
                Subject: Teeth
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Jaw
                Subject: Teeth
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Jaw
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Jaw
                Subject: Research and Analysis Methods
                Subject: Microscopy
                Subject: Electron Microscopy
                Subject: Scanning Electron Microscopy
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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