Ancestrally high elastic modulus of gecko setal β-keratin

Anne M Peattie () Carmel Majidi Andrew Corder Robert J Full 0 Present address: Department of Biomedical Engineering, University of Southern California, Denny Research Centre 140 , Los Angeles, CA 90089, USA 1 Department of Electrical Engineering and Computer Science, University of California , Berkeley , 333 Cory Hall, Berkeley, CA 94720-1770, USA 2 Department of Integrative Biology, University of California , Berkeley , 3060 Valley Life Sciences Building , Berkeley, CA 94720-3140, USA Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here - Email alerting service To subscribe to J. R. Soc. Interface go to: http://rsif.royalsocietypublishing.org/subscriptions Ancestrally high elastic modulus of gecko setal b-keratin Typical bulk adhesives are characterized by soft, tacky materials with elastic moduli well below 1 MPa. Geckos possess subdigital adhesives composed mostly of b-keratin, a relatively stiff material. Biological adhesives like those of geckos have inspired empirical and modelling research which predicts that even stiff materials can be effective adhesives if they take on a fibrillar form. The molecular structure of b-keratin is highly conserved across birds and reptiles, suggesting that material properties of gecko setae should be similar to that of b-keratin previously measured in birds, but this has yet to be established. We used a resonance technique to measure elastic bending modulus in two species of gecko from disparate habitats. We found no significant difference in elastic modulus between Gekko gecko (1.6 GPaG0.15 s.e.; nZ24 setae) and Ptyodactylus hasselquistii (1.4 GPaG0.15 s.e.; nZ24 setae). If the elastic modulus of setal keratin is conserved across species, it would suggest a design constraint that must be compensated for structurally, and possibly explain the remarkable variation in gecko adhesive morphology. 1. INTRODUCTION Geckos rapidly scale both vertical and inverted surfaces using fibrillar adhesive pads with some unique and impressive qualities. The adhesive is self-cleaning (Hansen & Autumn 2005) and strong, yet orientationdependent, allowing them to detach with minimal force (Autumn et al. 2000). Conventional pressure-sensitive adhesives (e.g. tape) are characterized by a relatively low Youngs modulus (less than 1 MPa; Dahlquist 1966), relying on the compliance of the material to create the intimate contact between surfaces necessary for intermolecular adhesion. Fibrillar adhesives are thought to rely instead on an array of high aspect ratio beams to form a structure that is effectively compliant while materially stiff (Autumn et al. 2006). The basic units of the gecko adhesive, called setae (figure 1) are composed predominantly of b-keratin (Maderson 1964; Alibardi 2003). The molecular structure and composition of b-keratin has been well characterized in bird feathers and scales (Gregg & Rogers 1984; Gregg et al. 1984), and mechanical testing has revealed feather keratin to be a relatively stiff material (approx. 2.50 GPa; Bonser & Purslow 1995), three orders of magnitude higher in Youngs modulus than the Dahlquist criterion for tack (figure 2). Surprisingly, few attempts have been made at characterizing the mechanical properties of b-keratin beyond research on bird feathers, despite the fact that it is found in all members of non-mammalian amniotes (figure 3). Among them, the material properties of gekkonid setal keratin have yet to be established. If synthetic fibrillar adhesives existed, we could directly manipulate their structure and material to determine how these parameters affect their performance. Such synthetic versions are in the works (Sitti & Fearing 2002; Geim et al. 2003; Northen & Turner 2005; Yurdumakan et al. 2005; Majidi et al. 2006), but in the meantime investigators have created mathematical models to predict the advantages of fibrillar adhesive design. This ongoing effort demands some estimate of the material properties of the modelled fibres. Since the basic molecular structure and composition of b-keratin is thought to be widely conserved across birds and reptiles (Fraser & Parry 1996; Sawyer et al. 2000), it is appropriate that most authors choose an estimate of Youngs modulus for gecko setal keratin between 1 and 4 GPa (Jagota & Bennison 2002; Campolo et al. 2003; Persson 2003; Gao & Yao 2004; Glassmaker et al. 2004; Majidi et al. 2005; Spolenak et al. 2005; Tang et al. 2005; Autumn et al. 2006), on the order of values found for feathers. Other estimates range up to 15 GPa (based on unpublished data; Sitti & Fearing 2003). This outstanding unknown parameter demands direct measurement owing to its importance in models Elastic modulus of gecko setal b-keratin A. M. Peattie et al. e u adiposemtisessogtlaepae tacky 1 kPa tce i l u tc c e s n ti f o s 100 kPa 1 MPa ) l o o ilinkeratin(ew ncrete res - bon co 1 GPa 1 TPa mammals lizards and snakes crocodiles of adhesion as well as understanding the materials evolution. Has natural selection optimized b-keratin for fibrillar adhesion, or do geckos possess the same b-keratin as their ancestors? Although the helical b-sheet structure of b-keratin is thought to be conserved, the underlying amino acids are not. Recent work by Alibardi (Alibardi & Toni 2005) suggests that geckos and birds converged independently on their keratinous fibrils (setae and feathers, respectively) by evolving low molecular weight b-keratins that are then polymerized into long filaments. Keratin filaments are in turn cross-linked together longitudinally by disulfide bonds (Rizzo et al. 2006). Increased cross-linkage could increase the material stiffness (Parbhu et al. 1999). Stiffness has also been found to depend on orientation of the keratin fibrils along the feather rachis (Cameron et al. 2003). Without direct measurements, there remains the possibility of variation in both the tensile and the bending moduli depending on what types of b-keratin molecules are manufactured and how they are assembled in the animal. Geckos have diverged ecologically such that they inhabit humid tropical as well as arid desert environments, and encompass both diurnally and nocturnally active species. If the material properties of setal b-keratin are variable, some species could conceivably benefit from evolutionary pressure driving changes in stiffness or viscoelasticity (e.g. through increased or decreased degrees of cross-linkage) to compensate for the effects of extreme environments. Alternatively, if material properties are constrained across gekkonids, that pressure could drive structural changes instead. Another important consideration is how setae age; depending on the species, a gecko must use the same setae for weeks or months between moults. Setae are not adhesive in their resting state, but must deform by bending to generate adhesive force (Autumn et al. 2000; Autumn & Hansen 2006). If material properties c (...truncated)