45
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Matrotrophy and placentation in invertebrates: a new paradigm

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          ABSTRACT

          Matrotrophy, the continuous extra‐vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy—placentotrophy—is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of ( i) local zones of enhanced nutritional transport (placental analogues), including specialized parent–offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, ( ii) compartmentalization of the common incubatory space into more compact and ‘isolated’ chambers with presumably more effective nutritional relationships, and ( iii) internal secretory (‘milk’) glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels—positional, structural and physiological.

          Related collections

          Most cited references139

          • Record: found
          • Abstract: found
          • Article: not found

          A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation.

          Beetles represent almost one-fourth of all described species, and knowledge about their relationships and evolution adds to our understanding of biodiversity. We performed a comprehensive phylogenetic analysis of Coleoptera inferred from three genes and nearly 1900 species, representing more than 80% of the world's recognized beetle families. We defined basal relationships in the Polyphaga supergroup, which contains over 300,000 species, and established five families as the earliest branching lineages. By dating the phylogeny, we found that the success of beetles is explained neither by exceptional net diversification rates nor by a predominant role of herbivory and the Cretaceous rise of angiosperms. Instead, the pre-Cretaceous origin of more than 100 present-day lineages suggests that beetle species richness is due to high survival of lineages and sustained diversification in a variety of niches.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Assessing the root of bilaterian animals with scalable phylogenomic methods.

            A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Phylogenomics revives traditional views on deep animal relationships.

              The origin of many of the defining features of animal body plans, such as symmetry, nervous system, and the mesoderm, remains shrouded in mystery because of major uncertainty regarding the emergence order of the early branching taxa: the sponge groups, ctenophores, placozoans, cnidarians, and bilaterians. The "phylogenomic" approach [1] has recently provided a robust picture for intrabilaterian relationships [2, 3] but not yet for more early branching metazoan clades. We have assembled a comprehensive 128 gene data set including newly generated sequence data from ctenophores, cnidarians, and all four main sponge groups. The resulting phylogeny yields two significant conclusions reviving old views that have been challenged in the molecular era: (1) that the sponges (Porifera) are monophyletic and not paraphyletic as repeatedly proposed [4-9], thus undermining the idea that ancestral metazoans had a sponge-like body plan; (2) that the most likely position for the ctenophores is together with the cnidarians in a "coelenterate" clade. The Porifera and the Placozoa branch basally with respect to a moderately supported "eumetazoan" clade containing the three taxa with nervous system and muscle cells (Cnidaria, Ctenophora, and Bilateria). This new phylogeny provides a stimulating framework for exploring the important changes that shaped the body plans of the early diverging phyla.
                Bookmark

                Author and article information

                Journal
                Biol Rev Camb Philos Soc
                Biol Rev Camb Philos Soc
                10.1111/(ISSN)1469-185X
                BRV
                Biological Reviews of the Cambridge Philosophical Society
                Blackwell Publishing Ltd (Oxford, UK )
                1464-7931
                1469-185X
                29 April 2015
                August 2016
                : 91
                : 3 ( doiID: 10.1111/brv.2016.91.issue-3 )
                : 673-711
                Affiliations
                [ 1 ] Department of Invertebrate Zoology, Faculty of BiologySaint Petersburg State University Universitetskaja nab. 7/9 199034 Saint PetersburgRussia
                [ 2 ] Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, GeozentrumUniversity of Vienna Althanstrasse 14 A‐1090 ViennaAustria
                [ 3 ] Integrative Research CenterField Museum of Natural History 1400 S. Lake Shore Dr. Chicago IL 60605U.S.A.
                [ 4 ]National Institute of Water and Atmospheric Research Private Bag 14901, Kilbirnie WellingtonNew Zealand
                [ 5 ] Department of Integrative Zoology, Faculty of Life SciencesUniversity of Vienna Althanstrasse 14 A‐1090 ViennaAustria
                [ 6 ] Department for Molecular Evolution and Development, Faculty of Life SciencesUniversity of Vienna Althanstrasse 14 A‐1090 ViennaAustria
                [ 7 ] Department of Embryology, Faculty of BiologySaint Petersburg State University Universitetskaja nab. 7/9 199034 Saint PetersburgRussia
                [ 8 ]Institut Méditerranéen de Biodiversité et d'Ecologie marine et continentale, Aix Marseille Université, CNRS, IRD, Avignon Université Station marine d'Endoume, Chemin de la Batterie des Lions 13007 MarseilleFrance
                Author notes
                [*] [* ]Address for correspondence (Tel.: +43 1 4277 53531, +7 812 692 05 30; E‐mail: andrei.ostrovsky@ 123456univie.ac.at ; oan_univer@ 123456yahoo.com ).
                Article
                BRV12189
                10.1111/brv.12189
                5098176
                25925633
                dbf9f492-fdd6-4ed3-b689-83131e7fd074
                © 2015 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 January 2014
                : 18 March 2015
                : 24 March 2015
                Page count
                Pages: 42
                Funding
                Funded by: Austrian Science Fund (FWF)
                Award ID: P22696‐B17
                Funded by: Russian Foundation for Basic Research (RFFI)
                Award ID: 10‐04‐00085‐a
                Award ID: 13‐04‐00758‐a
                Funded by: Saint Petersburg State University
                Award ID: 1.38.233.2015
                Funded by: French National Research Agency (CNRS) Labex OT‐Med
                Award ID: ANR‐11‐LABX‐0061
                Funded by: A*MIDEX
                Award ID: ANR‐11‐IDEX‐0001‐02
                Funded by: National Institute of Water and Atmospheric Research under Coasts and Oceans Research Programme 2, Marine Biological Resources: Discovery and definition of the marine biota of New Zealand
                Award ID: 2012/13 SCI
                Funded by: Negaunee Foundation
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                brv12189
                August 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.7 mode:remove_FC converted:09.11.2016

                Ecology
                matrotrophy,viviparity,brooding,placenta,invertebrates,convergent evolution
                Ecology
                matrotrophy, viviparity, brooding, placenta, invertebrates, convergent evolution

                Comments

                Comment on this article