Preprint Review Version 1 Preserved in Portico This version is not peer-reviewed

Convergent Evolution of Attachment Mechanisms in Aquatic Animals

These authors contributed equally to this work.
Version 1 : Received: 23 March 2022 / Approved: 24 March 2022 / Online: 24 March 2022 (07:20:55 CET)

How to cite: Delroisse, J.; Kang, V.; Gouveneaux, A.; Santos, R.; Flammang, P. Convergent Evolution of Attachment Mechanisms in Aquatic Animals. Preprints 2022, 2022030324 (doi: 10.20944/preprints202203.0324.v1). Delroisse, J.; Kang, V.; Gouveneaux, A.; Santos, R.; Flammang, P. Convergent Evolution of Attachment Mechanisms in Aquatic Animals. Preprints 2022, 2022030324 (doi: 10.20944/preprints202203.0324.v1).

Abstract

To resist hydrodynamic forces, two main underwater attachment strategies have evolved multiple times in aquatic animals: glue-like “bioadhesive secretions” and pressure-driven “suction attachment”. In this review, we use a multi-level approach to highlight convergence in underwater attachment mechanisms across four different length-scales (organism, organ, microscopic and molecular). At the organism level, the ability to attach may serve a variety of functions, the most important being: (i) positional maintenance, (ii) locomotion, (iii) feeding, (iv) building, and (v) defense. Aquatic species that use bioadhesive secretions have been identified in 28 metazoan phyla out of the 34 currently described, while suction organs have a more restricted distribution and have been identified in five phyla. Although biological adhesives are highly diverse, it is possible to categorize them into four main types according to the time scale of operation: permanent, temporary, transitory, and instantaneous adhesion. At the organ level some common principles have evolved independently in different biological lineages: for example, animals with single-unit attachment organs can be distinguished from those with multi-unit organs. Fundamental design elements can also be recognized for both types of attachment mechanisms. Suction attachment systems comprise a circular or elliptical attachment disc, a sealing rim to prevent leakage and a mechanism to lower the internal pressure. Bioadhesive-producing organs, on the other hand, usually contain a glandular tissue associated with connective tissues or other types of load-bearing support structures and muscles that facilitate locomotion or mechanical detachment. At the microscopic level, similar designs and organizations appear once again to have emerged independently in different phylogenetic lineages. Independent of the taxon and type of adhesion, there are species in which the biosynthesis, packaging and release of adhesive secretions takes place at the level of a single type of secretory cell, whereas in others these secretions are produced by two or more secretory cell types. Duo-gland adhesive systems involved in temporary adhesion present an additional level of complexity as they also exhibit de-adhesive secretory cells. Yet, strikingly similar cellular organizations have been reported in highly disparate species. In the case of biological suction organs, regions of the organ that contact the substratum are highly textured with stiff microstructures. Although clearly non-homologous in different animals, these microstructures are thought to enhance friction on rough surfaces. At the molecular level, proteins are the main organic constituent of adhesive secretions in aquatic animals. We compared the global amino acid compositions of bioadhesives using principal component analysis to show that homologous adhesives from phylogenetically related species cluster together, and there is little overlap between taxonomic groups. However, several non-permanent adhesives are grouped together even though they belong to disparate phyla, indicating convergence in amino acid composition. We also investigated relatedness among individual adhesive proteins using a sequence similarity-based clustering analysis. While many proteins appear taxon-specific, some have clear sequence homologies based on shared protein domains between phylogenetically distant organisms. However, it is highly probable that these domains, which are also present in many non-adhesive proteins, were convergently acquired from ancestral proteins with unrelated general functions. We herein present morphological, structural, and molecular convergences between different attachment mechanisms in aquatic animals that likely arose in response to shared functional and selective pressures.

Keywords

metazoans; adhesive organs; suction organs; functional morphology; adhesive proteins

Subject

BIOLOGY, Animal Sciences & Zoology

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