Biomimetics and evolution S. N. Patek Science 345, 1448 (2014); DOI: 10.1126/science.1256617
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Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
Downloaded from www.sciencemag.org on September 25, 2014
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INSIGHTS
CRISPR interference through kinky nucleotides p. 1452 Plasmid sequencing tracks antibiotic resistance p. 1454
PERSPECTIVES
A Tokay gecko (Gekko gecko). Adhesive strength. The remarkably adhesive feet of geckos are paved with microscopic setae, which enable them to run upside down on surfaces including glass.
MATERIALS SCIENCE
Biomimetics and evolution By S. N. Patek
B
iomimetics is based on the idea that living systems offer novel solutions to engineering challenges, as exemplified by the legendary story of how a stubbornly attached burr led to the development of Velcro. Yet, despite dramatic increases in biomimetic research, marketable products remain rare. Evolutionary analysis can be essential for pinpointing biological features that can be emulated in engineered structures. A recently published approach that links biomechanics and evolutionary analysis (1) points to a powerful 1448
strategy for biomimetics, as illustrated by the development of gecko-inspired adhesives (2, 3). Geckos are renowned for their ability to run upside down on ceilings and stick to glass. Biomimetic studies have mostly focused on the fine hairs (setae) covering gecko feet. The setae enable close surface contact, thus allowing adhesion to a wide range of surfaces without sticky secretions (4). However, a problem emerged for largescale fabrication: Biomimetic setae do not scale up to allow large forces (5, 6). Evolutionary analyses of setal scaling presaged these fabrication challenges by revealing
that setal adhesion does not fully explain the relationships between setal pad area, setal contact splitting, and animal body mass; the latter should correlate with adhesive properties, given that the feet must support body weight (7, 8). A team of researchers realized the import of these evolutionary studies, turned away from the prevailing focus on setae, and connected key insights from evolutionary analyses of adhesive scaling to the physics of adhesion (2, 3). They proposed and tested a scaling equation that relates the maximum adhesive force to the strength of the intermolecular bonds of the interface, the surface sciencemag.org SCIENCE
19 SEP TEMBER 2014 • VOL 345 ISSUE 6203
Published by AAAS
PHOTO: JOHN SOLEM/UNIVERSITY OF MASSACHUSETTS AT AMHERST
Linking biomechanical and evolutionary analysis helps to create viable biomimetic products
PHOTO: MICHAEL J. BARTLETT AND DANIEL R. KING/UNIVERSITY OF MASSACHUSETTS AT AMHERST
area of adhesion, and the comA B pliance, or inverse of stiffness, of the system (3, 9). The work led to the invention of Geckskin (developed at the University of Massacusetts Amherst), which combines fabric and soft materials, such as polydimethylsiloxane (PDMS), that can make contact at micrometer and submicrometer scales without the need for extremely fine fibers. Geckskin’s properties are ideal for effective, scalable adLearning from evolution. Many biomimetic studies hesion, providing a balance of have aimed to mimic setal adhesion. The developers draping and stiffness, abrupt of Geckskin instead used evidence from evolutionary detachment at a critical force analyses [see schematic in panel (A)] together with (unstable failure), and minimal a guiding equation of adhesive scaling to create an use of energy through optimal effective, dry adhesive. The material adheres so strongly elastic energy storage. These that a 100 cm2 pad can hold 300 kg (B). features differ from those of traditional fiber-reinforced adhesives, which focusing on the desired engineering outtypically use the viscoelasticity of the mateput (such as increasing adhesive force with rial for elastic energy transitions and require size of adhesive). The explanatory power of continuing force to achieve detachment this relationship is then tested by incorpo(stable failure) (2, 3). Geckskin materials rating data from multiple species. If the focan generate substantial adhesive forces, be cal biological variables do not fully explain scaled to large areas (see the figure), and be the relationship (for example, setal contact applied over a wide range of surface types splitting does not adequately explain adhe(2, 3, 10). In addition to circumventing the sive force), the deviation from the guiding setal-scaling issues, Geckskin products are equation (outside of measurement error) is dry (not sticky), cheap, reusable, scalable, considered equation error. Equation error and cleanable, fulfilling many of the goals of typically indicates an incorrect or incomsetal biomimetics. plete equation. The invention of Geckskin relied on key inRather than viewing equation error as sights from previous evolutionary analyses of problematic, Taylor and Thomas use it to adhesive scaling combined with the physics refine the hypothesized variables. For exof adhesion. Comparative studies are increasample, in gecko setal scaling studies, equaingly common in biomimetics (11, 12). Howtion error indicated that compliance and ever, statistical analyses that do not include compliant structures needed to be incorevolutionary analysis can result in spurious porated into the scaling equation. Equation correlations (13). For example, a comparaerror points to alternative mechanical hytive study of biological adhesion incorrectly potheses by indicating the presence of imreported a correlation between setal pad portant but unmeasured variables. It also area and body mass (14). Statistical and reveals the presence of shared variation methodological incorporation of evolutionin these variables among closely related ary relationships and multispecies data sets species. These evolutionary relationships is essential for correctly estimating correlaamong species can be used to correct for tions among traits, identifying the origins of the nonindependence of the data. By pintraits, and revealing the pathways and timing pointing shared variation in unmeasured of these relationships (13). Indeed, Geckskin variables that may also play distinct roles scaling analyses also need to statistically inin a subset of species, evolutionary analysis corporate phylogenetic relationships (10). is an important step toward finding good Taylor and Thomas (1) chart a path for a model species for biomimetics. robust evolutionary approach to biomechanTaylor and Thomas’ framework includes ics that can also be applied to the growing another key insight into the informaneed for quantitative evolutionary analysis tion provided by evolutionary analysis of in biomimetics. The first, and perhaps most mechanical systems. Biological systems difficult, step is to define equation-based retypically navigate a range of objectives delationships among the variables of interest, pending on their environment. When there are trade offs among traits in different environments, there can be multiple equally Biology Department, Duke University, Durham, NC 27708, effective solutions to these trade offs. CrossUSA. E-mail: [email protected] SCIENCE sciencemag.org
species studies provide a database of these equally effective solutions (called Pareto sets) that can be used for biomimetics. Variation in biological trait combinations across a range of conditions can inform biomimetic systems for use in specific environments or for particular functions. This approach to biomimetics demands a physical understanding of a system through equation-based analysis and a direct connection to biological features through both mechanical and evolutionary analysis. It can even incorporate environmental variation that maps to equally viable combinations of traits. For setal biomimetics, this approach could have more quickly focused efforts on solving the adhesive scaling conundrum. Further insight may come from studies showing that across gecko evolutionary history, setae originated and were lost repeatedly (15), suggesting varying utility of setal attachments under particular conditions. These data provide a rich evolutionary data set for defining suites of traits that are equally effective across a range of environmental settings or conditions. In this and other areas of biomimetics, recognizing the limitations of single-species studies and embracing the data set of evolutionary history will be key for achieving cost-effective and efficient translation from biology to marketable products. ■ REF ERENCES AND NOTES
1. G. K. Taylor, A. L. R. Thomas, Evolutionary Biomechanics, P. H. Harvey, R. M. May, H. C. J. Godfray, J. A. Dunne, Eds., Oxford Series in Ecology and Evolution (Oxford University Press, Oxford, 2014). 2. D. R. King, M. D. Bartlett, C. A. Gilman, D. J. Irschick, A. J. Crosby, Adv. Mater. 26, 4345 (2014). 3. M. D. Bartlett et al., Adv. Mater. 24, 1078 (2012). 4. K. Autumn, Am. Sci. 94, 124 (2006). 5. A. Parness et al., J. R. Soc. Interface 6, 1223 (2009). 6. L. Ge et al., Proc. Natl. Acad. Sci. U.S.A. 104, 10792 (2007). 7. D. J. Irschick et al., Biol. J. Linn. Soc. Lond. 59, 21 (1996). 8. A. M. Peattie, R. J. Full, Proc. Natl. Acad. Sci. U.S.A. 104, 18595 (2007). 9. M. D. Bartlett et al., Adv. Funct. Mater. 22, 4985 (2012). 10. M. D. Bartlett, A. J. Crosby, Adv. Mater. 26, 3405 (2014). 11. F. T. Malik, R. M. Clement, D. T. Gethin, W. Krawszik, A. R. Parker, Bioinspir. Biomim. 9, 031002 (2014). 12. G. Tokić, D. K. P. Yue, Proc. Biol. Sci. 279, 3065 (2012). 13. C. L. Nunn, The Comparative Approach in Evolutionary Anthropology and Biology (Univ. of Chicago Press, Chicago, 2011). 14. E. Arzt et al., Proc. Natl. Acad. Sci. U.S.A. 100, 10603 (2003). 15. T. Gamble et al., PLOS ONE 7, e39429 (2012). ACKNOWL EDGMENTS
I thank A. J. Crosby and D. Irschick and their research groups at the University of Massachusetts Amherst for providing images and members of the Patek Laboratory for their constructive feedback. 10.1126/science.1256617 19 SEP TEMBER 2014 • VOL 345 ISSUE 6203
Published by AAAS
1449
This copy is for your personal, non-commercial use only.
If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here.
The following resources related to this article are available online at www.sciencemag.org (this information is current as of September 25, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/345/6203/1448.full.html This article cites 13 articles, 5 of which can be accessed free: http://www.sciencemag.org/content/345/6203/1448.full.html#ref-list-1 This article appears in the following subject collections: Materials Science http://www.sciencemag.org/cgi/collection/mat_sci
Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
Downloaded from www.sciencemag.org on September 25, 2014
Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here.
INSIGHTS
CRISPR interference through kinky nucleotides p. 1452 Plasmid sequencing tracks antibiotic resistance p. 1454
PERSPECTIVES
A Tokay gecko (Gekko gecko). Adhesive strength. The remarkably adhesive feet of geckos are paved with microscopic setae, which enable them to run upside down on surfaces including glass.
MATERIALS SCIENCE
Biomimetics and evolution By S. N. Patek
B
iomimetics is based on the idea that living systems offer novel solutions to engineering challenges, as exemplified by the legendary story of how a stubbornly attached burr led to the development of Velcro. Yet, despite dramatic increases in biomimetic research, marketable products remain rare. Evolutionary analysis can be essential for pinpointing biological features that can be emulated in engineered structures. A recently published approach that links biomechanics and evolutionary analysis (1) points to a powerful 1448
strategy for biomimetics, as illustrated by the development of gecko-inspired adhesives (2, 3). Geckos are renowned for their ability to run upside down on ceilings and stick to glass. Biomimetic studies have mostly focused on the fine hairs (setae) covering gecko feet. The setae enable close surface contact, thus allowing adhesion to a wide range of surfaces without sticky secretions (4). However, a problem emerged for largescale fabrication: Biomimetic setae do not scale up to allow large forces (5, 6). Evolutionary analyses of setal scaling presaged these fabrication challenges by revealing
that setal adhesion does not fully explain the relationships between setal pad area, setal contact splitting, and animal body mass; the latter should correlate with adhesive properties, given that the feet must support body weight (7, 8). A team of researchers realized the import of these evolutionary studies, turned away from the prevailing focus on setae, and connected key insights from evolutionary analyses of adhesive scaling to the physics of adhesion (2, 3). They proposed and tested a scaling equation that relates the maximum adhesive force to the strength of the intermolecular bonds of the interface, the surface sciencemag.org SCIENCE
19 SEP TEMBER 2014 • VOL 345 ISSUE 6203
Published by AAAS
PHOTO: JOHN SOLEM/UNIVERSITY OF MASSACHUSETTS AT AMHERST
Linking biomechanical and evolutionary analysis helps to create viable biomimetic products
PHOTO: MICHAEL J. BARTLETT AND DANIEL R. KING/UNIVERSITY OF MASSACHUSETTS AT AMHERST
area of adhesion, and the comA B pliance, or inverse of stiffness, of the system (3, 9). The work led to the invention of Geckskin (developed at the University of Massacusetts Amherst), which combines fabric and soft materials, such as polydimethylsiloxane (PDMS), that can make contact at micrometer and submicrometer scales without the need for extremely fine fibers. Geckskin’s properties are ideal for effective, scalable adLearning from evolution. Many biomimetic studies hesion, providing a balance of have aimed to mimic setal adhesion. The developers draping and stiffness, abrupt of Geckskin instead used evidence from evolutionary detachment at a critical force analyses [see schematic in panel (A)] together with (unstable failure), and minimal a guiding equation of adhesive scaling to create an use of energy through optimal effective, dry adhesive. The material adheres so strongly elastic energy storage. These that a 100 cm2 pad can hold 300 kg (B). features differ from those of traditional fiber-reinforced adhesives, which focusing on the desired engineering outtypically use the viscoelasticity of the mateput (such as increasing adhesive force with rial for elastic energy transitions and require size of adhesive). The explanatory power of continuing force to achieve detachment this relationship is then tested by incorpo(stable failure) (2, 3). Geckskin materials rating data from multiple species. If the focan generate substantial adhesive forces, be cal biological variables do not fully explain scaled to large areas (see the figure), and be the relationship (for example, setal contact applied over a wide range of surface types splitting does not adequately explain adhe(2, 3, 10). In addition to circumventing the sive force), the deviation from the guiding setal-scaling issues, Geckskin products are equation (outside of measurement error) is dry (not sticky), cheap, reusable, scalable, considered equation error. Equation error and cleanable, fulfilling many of the goals of typically indicates an incorrect or incomsetal biomimetics. plete equation. The invention of Geckskin relied on key inRather than viewing equation error as sights from previous evolutionary analyses of problematic, Taylor and Thomas use it to adhesive scaling combined with the physics refine the hypothesized variables. For exof adhesion. Comparative studies are increasample, in gecko setal scaling studies, equaingly common in biomimetics (11, 12). Howtion error indicated that compliance and ever, statistical analyses that do not include compliant structures needed to be incorevolutionary analysis can result in spurious porated into the scaling equation. Equation correlations (13). For example, a comparaerror points to alternative mechanical hytive study of biological adhesion incorrectly potheses by indicating the presence of imreported a correlation between setal pad portant but unmeasured variables. It also area and body mass (14). Statistical and reveals the presence of shared variation methodological incorporation of evolutionin these variables among closely related ary relationships and multispecies data sets species. These evolutionary relationships is essential for correctly estimating correlaamong species can be used to correct for tions among traits, identifying the origins of the nonindependence of the data. By pintraits, and revealing the pathways and timing pointing shared variation in unmeasured of these relationships (13). Indeed, Geckskin variables that may also play distinct roles scaling analyses also need to statistically inin a subset of species, evolutionary analysis corporate phylogenetic relationships (10). is an important step toward finding good Taylor and Thomas (1) chart a path for a model species for biomimetics. robust evolutionary approach to biomechanTaylor and Thomas’ framework includes ics that can also be applied to the growing another key insight into the informaneed for quantitative evolutionary analysis tion provided by evolutionary analysis of in biomimetics. The first, and perhaps most mechanical systems. Biological systems difficult, step is to define equation-based retypically navigate a range of objectives delationships among the variables of interest, pending on their environment. When there are trade offs among traits in different environments, there can be multiple equally Biology Department, Duke University, Durham, NC 27708, effective solutions to these trade offs. CrossUSA. E-mail: [email protected] SCIENCE sciencemag.org
species studies provide a database of these equally effective solutions (called Pareto sets) that can be used for biomimetics. Variation in biological trait combinations across a range of conditions can inform biomimetic systems for use in specific environments or for particular functions. This approach to biomimetics demands a physical understanding of a system through equation-based analysis and a direct connection to biological features through both mechanical and evolutionary analysis. It can even incorporate environmental variation that maps to equally viable combinations of traits. For setal biomimetics, this approach could have more quickly focused efforts on solving the adhesive scaling conundrum. Further insight may come from studies showing that across gecko evolutionary history, setae originated and were lost repeatedly (15), suggesting varying utility of setal attachments under particular conditions. These data provide a rich evolutionary data set for defining suites of traits that are equally effective across a range of environmental settings or conditions. In this and other areas of biomimetics, recognizing the limitations of single-species studies and embracing the data set of evolutionary history will be key for achieving cost-effective and efficient translation from biology to marketable products. ■ REF ERENCES AND NOTES
1. G. K. Taylor, A. L. R. Thomas, Evolutionary Biomechanics, P. H. Harvey, R. M. May, H. C. J. Godfray, J. A. Dunne, Eds., Oxford Series in Ecology and Evolution (Oxford University Press, Oxford, 2014). 2. D. R. King, M. D. Bartlett, C. A. Gilman, D. J. Irschick, A. J. Crosby, Adv. Mater. 26, 4345 (2014). 3. M. D. Bartlett et al., Adv. Mater. 24, 1078 (2012). 4. K. Autumn, Am. Sci. 94, 124 (2006). 5. A. Parness et al., J. R. Soc. Interface 6, 1223 (2009). 6. L. Ge et al., Proc. Natl. Acad. Sci. U.S.A. 104, 10792 (2007). 7. D. J. Irschick et al., Biol. J. Linn. Soc. Lond. 59, 21 (1996). 8. A. M. Peattie, R. J. Full, Proc. Natl. Acad. Sci. U.S.A. 104, 18595 (2007). 9. M. D. Bartlett et al., Adv. Funct. Mater. 22, 4985 (2012). 10. M. D. Bartlett, A. J. Crosby, Adv. Mater. 26, 3405 (2014). 11. F. T. Malik, R. M. Clement, D. T. Gethin, W. Krawszik, A. R. Parker, Bioinspir. Biomim. 9, 031002 (2014). 12. G. Tokić, D. K. P. Yue, Proc. Biol. Sci. 279, 3065 (2012). 13. C. L. Nunn, The Comparative Approach in Evolutionary Anthropology and Biology (Univ. of Chicago Press, Chicago, 2011). 14. E. Arzt et al., Proc. Natl. Acad. Sci. U.S.A. 100, 10603 (2003). 15. T. Gamble et al., PLOS ONE 7, e39429 (2012). ACKNOWL EDGMENTS
I thank A. J. Crosby and D. Irschick and their research groups at the University of Massachusetts Amherst for providing images and members of the Patek Laboratory for their constructive feedback. 10.1126/science.1256617 19 SEP TEMBER 2014 • VOL 345 ISSUE 6203
Published by AAAS
1449
