<strong></strong>Convergent Evolution of Attachment Mechanisms in Aquatic Animals

Abstract

To resist hydrodynamic forces, two main underwater attachment strategies have evolved multiple times in aquatic animals: glue-like &amp;ldquo;bioadhesive secretions&amp;rdquo; and pressure-driven &amp;ldquo;suction attachment&amp;rdquo;. 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.

In the footsteps of sea stars: deciphering the catalogue of proteins involved in underwater temporary adhesion

“…Temporary adhesion can be defined as a reversible attachment process [ 14 ]. Many marine and freshwater organisms have developed temporary adhesion systems that show complexity at different length scales [ 15 ]. At the cellular level, adhesive secretions may be produced by one or more secretory cell types while, at the molecular level, the number and structure of adhesive proteins vary greatly from one taxonomic group to another [ 16 , 17 ].…”

Stickiness in shear: stiffness, shape, and sealing in bioinspired suction cups affect shear performance on diverse surfaces

“…To maintain stability in unpredictable environments, many aquatic organisms have evolved diverse attachment organs that anchor them to substrates. Attachment mechanisms such as suction, bioadhesives, and frictional elements can stabilize these organisms against forces introduced through crashing waves, strong directional flows, and predation [1][2][3]. In particular, the use of suction organs for aquatic adhesion has been described in multiple groups including various fish [2,4,5], cephalopods [6,7], and even freshwater insects [8][9][10][11].…”

“…In addition to providing rigidity, the arrangement of these bony structures can change the overall shape of the disc, producing forms that are more elliptical or ovate [3,21]. This shape can be further defined by additional features such as the presence of a soft rim, which may affect the overall design of the contacting disc margin (e.g.…”

Stiff skin, soft core: soft backings enhance the conformability and friction of fibre-reinforced adhesives

“…Bioadhesion research aims to sharpen our understanding of the complex physico-chemical mechanisms that underlie this striking performance, which is relevant to both fundamental and applied scientific research. On the one hand, insights into the functioning of bioadhesive systems contribute to an assessment of the evolutionary history of these animals [8][9][10][11]. On the other hand, the remarkable performance of bioadhesive systems has motivated the design of various biomimetic technologies, such as tree-frog-inspired adhesives [12], gecko-inspired climbing robots [13], soft robotic grippers [14] and bioinspired surgical instruments [15].…”