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Gecko Adhesion in Space and Time: A Phylogenetic Perspective on the Scansorial Success Story

Published on Jul 1, 2019in Integrative and Comparative Biology3.101
· DOI :10.1093/ICB/ICZ020
A M Bauer1
Estimated H-index: 1
(Villanova University)
Sources
Abstract
: An evolutionary perspective on gecko adhesion was previously hampered by a lack of an explicit phylogeny for the group and of robust comparative methods to study trait evolution, an underappreciation for the taxonomic and structural diversity of geckos, and a dearth of fossil evidence bearing directly on the origin of the scansorial apparatus. With a multigene dataset as the basis for a comprehensive gekkotan phylogeny, model-based methods have recently been employed to estimate the number of unique derivations of the adhesive system and its role in lineage diversification. Evidence points to a single basal origin of the spinulate oberhautchen layer of the epidermis, which is a necessary precursor for the subsequent elaboration of a functional adhesive mechanism in geckos. However, multiple gains and losses are implicated for the elaborated setae that are necessary for adhesion via van der Waals forces. The well-supported phylogeny of gekkotans has demonstrated that convergence and parallelism in digital design are even more prevalent than previously believed. It also permits the reexamination of previously collected morphological data in an explicitly evolutionary context. Both time-calibrated trees and recently discovered amber fossils that preserve gecko toepads suggest that a fully-functional adhesive apparatus was not only present, but also represented by diverse architectures, by the mid-Cretaceous. Further characterization and phylogenetically-informed analyses of the other components of the adhesive system (muscles, tendons, blood sinuses, etc.) will permit a more comprehensive reconstruction of the evolutionary pathway(s) by which geckos have achieved their structural and taxonomic diversity. A phylogenetic perspective can meaningfully inform functional and performance studies of gecko adhesion and locomotion and can contribute to advances in bioinspired materials.
  • References (115)
  • Citations (7)
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References115
Newest
#1Lorenzo Alibardi (UNIBO: University of Bologna)H-Index: 36
The digital adhesive pads that allow gecko lizards to climb vertical surfaces result from the modification of the oberhautchen layer of the epidermis in normal scales. This produces sticky filaments of 10–100 μm in length, called setae that are composed of various proteins. The prevalent types, termed corneous beta proteins (CBPs), have a low molecular weight (12–20 kDa) and contain a conserved central region of 34 amino acids with a beta-conformation. This determines their polymerization into l...
11 CitationsSource
#1Gabriela Fontanarrosa (CONICET: National Scientific and Technical Research Council)H-Index: 4
#2Juan D. Daza (SHSU: Sam Houston State University)H-Index: 15
Last. Virginia Abdala (CONICET: National Scientific and Technical Research Council)H-Index: 20
view all 3 authors...
Abstract Gekkota (geckos and pygopodids) is a clade thought to have originated in the Early Cretaceous and that today exhibits one of the most remarkable scansorial capabilities among lizards. Little information is available regarding the origin of scansoriality, which subsequently became widespread and diverse in terms of ecomorphology in this clade. An undescribed amber fossil (MCZ R–190835) from mid-Cretaceous outcrops of the north of Myanmar dated at 99 Ma, previously assigned to stem Gekkot...
8 CitationsSource
#1Paul M. Oliver (ANU: Australian National University)H-Index: 15
#2Rafe M. Brown (KU: University of Kansas)H-Index: 35
Last. Cameron D. Siler (OU: University of Oklahoma)H-Index: 22
view all 6 authors...
Regions with complex geological histories often have diverse and highly endemic biotas, yet inferring the ecological and historical processes shaping this relationship remains challenging. Here, in the context of the taxon cycle model of insular community assembly, we investigate patterns of lineage diversity and habitat usage in a newly characterized vertebrate radiation centred upon the world9s most geologically complex insular region: island arcs spanning from the Philippines to Fiji. On isla...
14 CitationsSource
#1Lida Xing (China University of Geosciences)H-Index: 20
#2Jingmai K. O’Connor (CAS: Chinese Academy of Sciences)H-Index: 29
Last. Ming Bai (CAS: Chinese Academy of Sciences)H-Index: 16
view all 7 authors...
Abstract Burmese amber has recently provided some detailed glimpses of plumage, soft tissues, and osteology of juvenile enantiornithine birds, but these insights have been restricted to isolated wing apices. Here we describe nearly half of a hatchling individual, based on osteological and soft tissue data obtained from the skull, neck, feet, and wing, and identified as a member of the extinct avian clade Enantiornithes. Preserved soft tissue provides the unique opportunity to observe the externa...
39 CitationsSource
#1Tony Gamble (Marquette University)H-Index: 22
#2Eli Greenbaum (UTEP: University of Texas at El Paso)H-Index: 23
Last. Aaron M. Bauer (Villanova University)H-Index: 34
view all 5 authors...
We published a phylogenetic comparative analysis that found geckos had gained and lost adhesive toepads multiple times over their long evolutionary history (Gamble et al. 2012). This was consistent with decades of morphological studies showing geckos had evolved adhesive toepads on multiple occasions and that the morphology of geckos with ancestrally padless digits can be distinguished from secondarily padless forms. Recently, Harrington and Reeder (2017) reanalyzed data from Gamble et al. (2012...
10 CitationsSource
#1Sean M. Harrington (SDSU: San Diego State University)H-Index: 5
#2Tod W. Reeder (SDSU: San Diego State University)H-Index: 31
The binary-state speciation and extinction (BiSSE) model has been used in many instances to identify state-dependent diversification and reconstruct ancestral states. However, recent studies have shown that the standard procedure of comparing the fit of the BiSSE model to constant-rate birth-death models often inappropriately favors the BiSSE model when diversification rates vary in a state-independent fashion. The newly-developed HiSSE model enables researchers to identify state-dependent diver...
14 CitationsSource
#1Anthony P. Russell (U of C: University of Calgary)H-Index: 39
#2M.‐J. Delaugerre (Conservatoire du littoral)H-Index: 1
Two distinctive patterns of adhesive toepad are found in the Gekkota – terminal leaf-like pads situated at the distal ends of the digits, and basal pads that encroach more proximally along the digits, are proportionally larger and are associated with more than just the ungual and distal portion of the penultimate phalanges. Although these two configurations have long been recognized, there has been no explanation of whether or not they are functionally different. A small offshore island provided...
12 CitationsSource
#1Lida Xing (China University of Geosciences)H-Index: 20
#2Ryan C. McKellar (University of Regina)H-Index: 15
Last. Philip J. Currie (U of A: University of Alberta)H-Index: 53
view all 14 authors...
Summary In the two decades since the discovery of feathered dinosaurs [1–3], the range of plumage known from non-avialan theropods has expanded significantly, confirming several features predicted by developmentally informed models of feather evolution [4–10]. However, three-dimensional feather morphology and evolutionary patterns remain difficult to interpret, due to compression in sedimentary rocks [9, 11]. Recent discoveries in Cretaceous amber from Canada, France, Japan, Lebanon, Myanmar, an...
59 CitationsSource
#1Timothy E. Higham (UCR: University of California, Riverside)H-Index: 27
#2Tony Gamble (Marquette University)H-Index: 22
Last. Anthony P. Russell (U of C: University of Calgary)H-Index: 39
view all 3 authors...
The evolutionary history of vertebrate locomotion is punctuated by innovations that have permitted expansion into novel ecological niches. Frictional adhesion of geckos is an innovation renowned for enabling locomotion on vertical and inverted smooth surfaces. Much is known about the microstructure and function of the fully-expressed gekkotan adhesive apparatus, although how it originated is poorly understood. Therefore, identifying species that exhibit the earliest stages of expression of frict...
18 CitationsSource
#1Anthony P. Russell (U of C: University of Calgary)H-Index: 39
#2Garrett S. Oetelaar (U of C: University of Calgary)H-Index: 1
Geckos with subdigital adhesive pads can scale smooth vertical surfaces in defiance of gravity. The deployment of the adhesive system is activated by the musculoskeletal system during active traverses of such surfaces, but adhesion on such substrata can also be achieved by passive means, with the body weight of the gecko applying tensile loading to the adhesive setae, maintaining prolonged, static contact with the surface. To investigate whether passively induced adhesion is employed by geckos h...
17 CitationsSource
Cited By7
Newest
#1Lorenzo Alibardi (UNIBO: University of Bologna)H-Index: 36
The formation of the complex pattern of setae in adhesive pads of geckos and anoline lizards has been analyzed by ultrastructural, autoradiographic, and immunohistochemical methods. Setae terminate with spatulated ends responsible for adhesion that allow these lizards to climb vertical substrates and conquer arboreal niches. Setae derive from a complex interfaced molding between two specialized epidermal layers of the shedding complex that determines the cyclical skin molting, Oberhautchen and c...
Source
#1Peter Uetz (VCU: Virginia Commonwealth University)H-Index: 40
#2Alex Slavenko (TAU: Tel Aviv University)H-Index: 1
Last. Matthew HeinickeH-Index: 1
view all 4 authors...
1 CitationsSource
#1Lorenzo Alibardi (UNIBO: University of Bologna)H-Index: 36
Adhesive pads of geckos contain many thousands of nanoscale spatulae for the adhesion and movement along vertical or inverted surfaces. Setae are composed of interlaced corneous bundles made of small cysteine-glycine-rich corneous beta proteins (CBPs, formerly indicated as beta-keratins), embedded in a matrix material composed of cytoskeletal proteins and lipids. Negatively charged intermediate filament keratins (IFKs) and positively charged CBPs likely interact within setae, aside disulphide bo...
Source
#1Shai Meiri (AMNH: American Museum of Natural History)H-Index: 36
6 CitationsSource
#1Anthony P. Russell (U of C: University of Calgary)H-Index: 39
#2Alyssa Y. Stark (Villanova University)H-Index: 11
Last. Timothy E. Higham (UCR: University of California, Riverside)H-Index: 27
view all 3 authors...
: Geckos are remarkable in their ability to reversibly adhere to smooth vertical, and even inverted surfaces. However, unraveling the precise mechanisms by which geckos do this has been a long process, involving various approaches over the last two centuries. Our understanding of the principles by which gecko adhesion operates has advanced rapidly over the past 20 years and, with this knowledge, material scientists have attempted to mimic the system to create artificial adhesives. From a biologi...
9 CitationsSource
#1Emily R Naylor (UCR: University of California, Riverside)H-Index: 1
#2Timothy E. Higham (UCR: University of California, Riverside)H-Index: 27
: Attachment is imperative for many biological functions, such as holding position and climbing, but can be challenged by natural conditions. Adhesive toe pads and claws have evolved in multiple terrestrial lineages as important dynamic attachment mechanisms, and some clades (e.g., geckos) exhibit both features. The functional relationship of these features that comprise a complex attachment system is not well-understood, particularly within lizards (i.e., if pads and claws are redundant or mult...
7 CitationsSource
#1Timothy E. Higham (UCR: University of California, Riverside)H-Index: 27
#2Anthony P. Russell (U of C: University of Calgary)H-Index: 39
Last. Thomas Speck (University of Freiburg)H-Index: 35
view all 5 authors...
: The study of gecko adhesion is necessarily interdisciplinary due to the hierarchical nature of the adhesive system and the complexity of interactions between the animals and their habitats. In nature, geckos move on a wide range of surfaces including soft sand dunes, trees, and rocks, but much of the research over the past two decades has focused on their adhesive performance on artificial surfaces. Exploring the complex interactions between geckos and their natural habitats will reveal aspect...
7 CitationsSource