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1. Convergent developmental patterns underlie the repeated evolution of adhesive toe pads among lizards

   https://doi.org/10.1093/biolinnean/blab164  

   Griffing, Aaron H ; Gamble, Tony ; Cohn, Martin J ; Sanger, Thomas J ( January 2022 , Biological Journal of the Linnean Society)

   Abstract How developmental modifications produce key innovations, which subsequently allow for rapid diversification of a clade into new adaptive zones, has received much attention. However, few studies have used a robust comparative framework to investigate the influence of evolutionary and developmental constraints on the origin of key innovations, such as the adhesive toe pad of lizards. Adhesive toe pads evolved independently at least 16 times in lizards, allowing us to examine whether the patterns observed are general evolutionary phenomena or unique, lineage-specific events. We performed a high-resolution comparison of plantar scale development in 14 lizard species in Anolis and geckos, encompassing five independent origins of toe pads (one in Anolis, four in geckos). Despite substantial evolutionary divergence between Anolis and geckos, we find that these clades have undergone similar developmental modifications to generate their adhesive toe pads. Relative to the ancestral plantar scale development, in which scale ridges form synchronously along the digit, both padded geckos and Anolis exhibit scansor formation in a distal-to-proximal direction. Both clades have undergone developmental repatterning and, following their origin, modifications in toe pad morphology occurred through relatively minor developmental modifications, suggesting that developmental constraints governed the diversification of the adhesive toe pad in lizards. 

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2. A Physical Model Approach to Gecko Adhesion Opportunity and Constraint: How Rough Could It Be?

   https://doi.org/10.1093/icb/icz029  

   Niewiarowski, Peter H. ; Dhinojwala, Ali ; Garner, Austin M. ( May 2019 , Integrative and Comparative Biology)

   It has been nearly 20 years since Autumn and colleagues established the central role of van der Waals intermolecular forces in how geckos stick. Much has been discovered about the structure and function of fibrillar adhesives in geckos and other taxa, and substantial success has been achieved in translating natural models into bioinspired synthetic adhesives. Nevertheless, synthetics still cannot match the multidimensional performance observed in the natural gecko system that is simultaneously robust to dirt and water, resilient over thousands of cycles, and purportedly competent on surfaces that are rough at drastically different length scales. Apparent insensitivity of adhesion to variability in roughness is particularly interesting from both a theoretical and applied perspective. Progress on understanding the extent to which and the basis of how the gecko adhesive system is robust to variation in roughness is impeded by the complexity of quantifying roughness of natural surfaces and a dearth of data on free-ranging gecko substrate use. Here we review the main challenges in characterizing rough surfaces as they relate to collecting relevant estimates of variation in gecko adhesive performance across different substrates in their natural habitats. In response to these challenges, we propose a practical protocol (borrowing from thermal biophysical ecological methods) that will enable researchers to design detailed studies of structure–function relationships of the gecko fibrillar system. Employing such an approach will help provide specific hypotheses about how adhesive pad structure translates into a capacity for robust gecko adhesion across large variation in substrate roughness. Preliminary data we present on this approach suggest its promise in advancing the study of how geckos deal with roughness variation. We argue and outline how such data can help advance development of design parameters to improve bioinspired adhesives based on the gecko fibrillar system.

    

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3. Shoulder joint range of motion in fossil synapsids and the origins of mammalian locomotor diversity

   Brocklehurst, R. J. ( July 2020 , Journal of Vertebrate Paleontology, Program and Abstracts, 2020)

   null (Ed.)

   Extant mammals are both taxonomically and ecologically diverse, having evolved a remarkable array of locomotor ecologies (e.g., swimming, digging, and flying). Evolution of the therian-type forelimb, with a highly reduced pectoral girdle and ball-and-socket shoulder joint, has been heralded as a key innovation that enabled mammals to co-opt their forelimbs for diverse functions. The acquisition of the mammal forelimb can be traced through their forerunners, the non-mammalian synapsids (NMS), but exactly how this musculoskeletal transformation proceeded and its impact on functional diversification have not be quantitatively tested. To explore the evolution of forelimb functional diversity in synapsids, we measured shoulder joint osteological range of motion (ROM) in a range of extant amniotes (lizards, monotremes, therian mammals), and compared their patterns of joint mobility to exemplars from each of the major grades of NMS: ‘pelycosaurs’, basal therapsids, and non-mammalian cynodonts. Three-dimensional models of the shoulder girdles and humeri were digitally aligned in an anatomical ‘neutral pose’ using a semi-automated approach based on articular surface morphology. ROM was then determined for the shoulder joint using a fully automated method, where the humerus was moved in flexion-extension, adduction-abduction, and pronation-supination until bone-to-bone contact occurred. Relative degree and directionality of mobility were then compared across taxa. We find an increase in total shoulder joint ROM through synapsid evolution, suggesting that more derived NMS could perform a wider range of limb movements. However, we also see more complex trends in directionality of shoulder mobility that may be indicators of forelimb posture. Extant lepidosaurs and monotremes had the greatest ROM in abduction-adduction, whereas therians had more ROM in flexion-extension, likely related to ‘sprawling’ vs. ‘erect’ gaits. Therapsids and cynodonts both had greatest ROM in abduction-adduction, matching previous reconstructions of these taxa as sprawling to semi-erect. However, ‘pelycosaurs’ had the greatest ROM in flexion-extension, despite having abducted forelimbs, suggesting they did not move their forelimbs in same manner as modern sprawling animals. Our results demonstrate the complex nature of forelimb evolution in synapsids and provide novel insights into the functional transformation and diversification of the mammalian forelimb. Funding Sources Funding information: NSF DEB- 1757749 (S.E.P) and NSF DEB-1754502 (K.D.A). 

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4. The development of cephalic armor in the tokay gecko (Squamata: Gekkonidae: Gekko gecko )

   https://doi.org/10.1002/jmor.21092  

   Laver, Rebecca J. ; Morales, Cristian H. ; Heinicke, Matthew P. ; Gamble, Tony ; Longoria, Kristin ; Bauer, Aaron M. ; Daza, Juan D. ( December 2019 , Journal of Morphology)

   Armored skin resulting from the presence of bony dermal structures, osteoderms, is an exceptional phenotype in gekkotans (geckos and flap‐footed lizards) only known to occur in three genera:Geckolepis,Gekko, andTarentola. The Tokay gecko (Gekko geckoLINNAEUS 1758) is among the best‐studied geckos due to its large size and wide range of occurrence, and although cranial dermal bone development has previously been investigated, details of osteoderm development along a size gradient remain less well‐known. Likewise, a comparative survey of additional species within the broaderGekkoclade to determine the uniqueness of this trait has not yet been completed. Here, we studied a large sample of gekkotans (38 spp.), including 18 specimens ofG. gecko, using X‐rays and high‐resolution computed tomography for visualizing and quantifying the dermal armorin situ. Results from this survey confirm the presence of osteoderms in a second species within this genus,GekkoreevesiiGRAY 1831, which exhibits discordance in timing and pattern of osteoderm development when compared with its sister taxon,G. gecko. We discuss the developmental sequence of osteoderms in these two species and explore in detail the formation and functionality of these enigmatic dermal ossifications. Finally, we conducted a comparative analysis of endolymphatic sacs in a wide array of gekkotans to explore previous ideas regarding the role of osteoderms as calcium reservoirs. We found thatG. geckoand other gecko species with osteoderms have highly enlarged endolymphatic sacs relative to their body size, when compared to species without osteoderms, which implies that these membranous structures might fulfill a major role of calcium storage even in species with osteoderms.

    

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5. Duplications in corneous beta protein genes and the evolution of gecko adhesion

   https://doi.org/doi:10.1093/icb/icz010  

   Gamble, T. ( January 2019 , Integrative and comparative biology)

   Corneous proteins are an important component of the tetrapod integument. Duplication and diversification of keratins and associated proteins are linked with the origin of most novel integumentary structures like mammalian hair, avian feathers, and scutes covering turtle shells. Accordingly, the loss of integumentary structures often coincides with the loss of genes encoding keratin and associated proteins. For example, many hair keratins in dolphins and whales have become pseudogenes. The adhesive setae of geckos and anoles are composed of both intermediate filament keratins (IF-keratins, formerly known as alpha-keratins) and corneous beta-proteins (CBPs, formerly known as beta-keratins) and recent whole genome assemblies of two gecko species and an anole uncovered duplications in seta-specific CBPs in each of these lineages. While anoles evolved adhesive toepads just once, there are two competing hypotheses about the origin(s) of digital adhesion in geckos involving either a single origin or multiple origins. Using data from three published gecko genomes, I examine CBP gene evolution in geckos and find support for a hypothesis where CBP gene duplications are associated with the repeated evolution of digital adhesion. Although these results are preliminary, I discuss how additional gecko genome assemblies, combined with phylogenies of keratin and associated protein genes and gene duplication models, can provide rigorous tests of several hypotheses related to gecko CBP evolution. This includes a taxon sampling strategy for sequencing and assembly of gecko genomes that could help resolve competing hypotheses surrounding the origin(s) of digital adhesion. 

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