Increasingly-free Artificial Life and Life-compatible Electronics

Here is yet another opportunity [1] to get A(rtificial) Life. For free. The proceedings of ECAL 2013 (the biennial European Artificial Life conference) is now available from MIT Press.

Now is your chance to learn about the latest advances in adaptive hardware, artificial immune systems, bioinspired robotics/learning, in silico evolution, and much more.....

In semi-related news, check out this video about flexible circuit design (their application is called "imperceptible circuits") from Digitized Information. And in increasingly tangential news, find out more about physically transient electronics [2] that are reabsorbed by the body when no longer needed [3]. 

An electrochemical schematic of a flexible electronic circuitry. Courtesy Figure 1 from [3]. 

NOTES:

[1] The proceedings for the Alife XI, Alife XII, Alife XIII conferences are also available.

[2] A biocompatible and potentially flexible circuitry that could be used for multiple applications in the field of bioelectronics. 

For more information, please see: Hwang et.al A Physically Transient Form of Silicon Electronics.  Science, 337, 1640 (2012).

[3] For more information, listen to this podcast with John Rogers at UIUC. This work is also part of a DARPA initiative in the area of  transparent conducting films. 

Algorithmic Self-assembly (with DNA) Profile

Another popular post that is being re-posted from my microblog, Tumbld Thoughts (on Algorithmic Self-assembly).

Here is David Doty (Math/CS) from Caltech discussing the theory of Algorithmic Self-Assembly [1] featured in a Communications of the ACM article — picture on the left, and Vimeo video slideshow — picture on the right). Here is a related blog post from 80 Beats (Discover magazine science blog) on DNA LEGO bricks. Enjoy both.

Associated trivia: the “Abstract Tile Assembly Model” [2] featured in the Vimeo video was developed by Erik Winfree (another DNA Computing person), who is the son of Arthur Winfree. Art Winfree wrote an excellent book called the “Geometry of Biological Time”, and was a mentor of Steven Strogatz [3].

NOTES:

[1] process by which “things autonomously (no directedness) assemble themselves into larger functional units”.

[2] for a demo, try out the the Xgrow simulator.

[3] a nice story about this is featured in the book “Sync”

Topological references, courtesy of Futurama

I am re-posting this from my microblog Tumbld Thoughts, as it has been one of my most popular posts there.  The theme fits in well with this blog as well.

Currently catching up on TV. In the Futurama episode "Benderama", there was a reference to the Banach-Tarski paradox (in the form of a duplicator machine) [1]. The machine is used to duplicate things (ultimately Bender) at progressively smaller scales [2]. All this in 23 minutes. Great stuff.

NOTES: 

[1] the point was not to be technically accurate. The point was to make an analogical and highly obscure reference so that people like me could talk about it.

[2]  the "shrinker" eventually leads to the potential destruction of the world's drinking supply (nice subreference to the gray goo hypothesis/scenario in the field of nanotechnology).

Merging electronics and biology: the future of touch

The sense of touch, or haptic perception, is a key feature of animal behavior. For humans, haptic perception and proprioception is a subtle but fundamental sensory modality that helps us move, plan, and interact with our environment. Recent developments in virtual environments and conformal electronics may allow us to build artificial sensory systems that fully integrate into the user’s neural function. But first, we must bring together a number of emerging themes in the scientific literature.

Multisensory Perception and the Sensory Milieu
To understand how the nervous system will deal with inputs from artificial touch sensors, we need to understand how the touch systems of the body behave when perturbed. Virtual reality systems specialized for creating sensory illusions are needed to uncover how visual and haptic information are collated at the body’s surface and merged in the brain (for example, see Figure 1). The integration of visual and touch cues can be explored in an active touch task [1]. In this example (Figure 1), force feedback is provided that corresponds with presented visual stimuli. Multisensory integration can also be explored and decoupled by examining changes in postural sway [1a] when the frequency of visual and touch cues are incongruent [2]. The integration of these signals in the mammalian brain is a stochastic process, involving integration sites such as the superior colliculus (SC) and posterior parietal cortex (PPC) [2a].

Studies examining the cell biology of cutaneous touch receptors at the skin surface have found that different populations of cells have different thresholds for activation [3], which is likely related to the complexity of information that the touch sensory modality provides. Much as the brain abstracts away the key pieces of information needed to perform specific tasks, robotic models have also been constructed to understand the core contributions of touch to multisensory perception [4]. This issue of minimal bandwidth requirements will be an important consideration in the design of future artificial touch systems. While relatively low amounts of information may actually be required for straightforward tasks (such as picking up a cup), a much greater amount of information (and perhaps noise as well) may be required for outcomes such as self-awareness or balance.

Figure 1. Experiment demonstrating the importance of coordinating and 

integrating vision and touch in exploration of unfamiliar objects. COURTESY: Figure 1 of [1].

The sensory milieu refers to myriad interactions between the major sensory systems of the brain (e.g. visual, touch, auditory) and the physiological mechanisms which underlie perception and action. The term "milieu" implies that homeostatic mechanisms are at play in these processes. Considering the emergent order and role of autoregulation among sensory inputs during integration and information processing is a novel way to view the neurobiology of sensation and perception. However, it may be useful to the design and maintenance of artificial systems for two reasons:

1) while it is clear what environmental information is required for statistically optimal perceptual performance [4a], in engineering contexts we may want to achieve sub-optimal performance or robust responses.

2) the perturbation (e.g. decoupling of visual and haptic information) of a multisensory system does not result in a total loss of perceptual integration, particularly over time. Therefore, there must be some type of homeostatic mechanism at play with respect to incoming sensory information [4b].

Artificial Touch is a Matter of Compliance

The interaction with the body’s surface is another key feature of artificial touch systems. To this extent, research that characterizes interactions between the physical properties of surfaces and touch systems is important (see Figure 2). Recent investigations into interactions between the epidermal ridges on the fingertip and the peaks and troughs of a rough surface show that surface forces become more variable with increases in roughness [5]. This leads to an increase in friction during sliding and other fine manipulation behaviors. This has consequences not only for the design of artificial touch systems, but for the tribological design of materials at multiple scales as well [5a].

Figure 2. The interaction between surface reaction forces and the dynamic biomechanics of touch (e.g. the interaction between the finger’s skin and the surface roughness). COURTESY: Figure 1 of [5].

Artificial touch systems require a range of novel material types. In robotics, it has become increasingly clear that the use of compliant (e.g. soft, biocompatible) materials are required for effective interaction [6]. Figure 3 demonstrates how the results shown in Figure 2 can be modulated through the manipulation of surface texture. By controlling the scale and geometry of surface features, friction due to sliding can be minimized. Looking forward (and to animal models), specialized surface features at multiple size scales can enable quite amazing functional behaviors [7].

Figure 3. An example of how surface texture can modulate surface reaction forces encountered at the fingertip. The phenomenon leads to our perception of different surface qualities (e.g. edges, orientation, smoothness). COURTESY: Figures 1 and 2 in [8].

In [8], an experiment using a sliding cantilever and a patterned elastomer demonstrated that the sliding motion of a fingertip can act to modulate the surface reaction force encountered during finger strike. The forces involved are small relative to forces encountered while walking or running [9]. However, the fingertip encounters strains which, when coupled with the complex curves of fingertip geometry, makes for an interesting design challenge. What is needed is a thin film that conducts electrical potentials, and that can bend or buckle without damage to the surface. The group in [10] have developed a carbon nanotube (CNT)-based solution to this problem. Embedded in their thin film piezoelectric device are CNT structures which store strain forces applied to the surface like a spring - and releases this potential after loading. The result is a stretchable capacitor that has the characteristics of a biological viscoelastic (e.g. skin-like) surface.

Figure 4. An summary of piezoelectric characterization for an electronic sensor device that covers the hand. COURTESY: Figure 5 in [11].

Figure 4 shows how such a thin, stretchable film might be used as a skin surrogate. The authors of [11] have engaged in extensive characterization of these types of surfaces. When the thumb is bent, a piezoelectric signal is generated that could be interfaced with the nervous system.

Conformal Electronics

In the past few years, compliant materials have been effectively used as a substrate for nanoelectronic arrays.  One of the leading innovators in this field is the Rogers group at UIUC, who have published a number of papers on fabricating (see Figures 5 and 6) and demonstrating the function (Figure 7) of these materials. One  commonly used fabrication technique involves the use of the silicon polymer Polydimethylsiloxane (PDMS) as a substrate. PDMS has many desirable properties for a device that will be embedded into the human body. That being said, there are other (and perhaps better) organic materials that could be used as a substrate. However, PDMS is the most common. For a presentation on the promise of tissue fabrication and potential methods, see [12].

Figure 5. An overview of how conformal electronics are fabricated. COURTESY: Figure 1 in [13].

Figure 6. The fabrication of microstructured PDMS films. COURTESY: Figure 1 in [14].

The fabrication process of a conformal electronic device can be seen in Figure 6, and shows how the thin film is molded and etched (embedded with features). In the end, we have a fully-functional and bendable array. Bendable electronics can be used for a range of applications, and is the enabling technology behind flexible OLED displays (perhaps a staple of third and fourth generation e-readers). Theoretically at least, a similar process could be used to fabricate multi-layered embeddable replacement skins for humans, which could not only restore the function of touch but also augment our sensory capabilities. A number of challenges would have to be overcome, including interfaces with the body's endocrine (hormones), circulatory (blood), and excretory (sweat) systems, the importance of which is discussed in [15].

Figure 7. An overview of the deformational and functional properties of conformal electronics. COURTESY: Figure 2 in [13].

The Future

Through the use of compliant and biocompatible materials, algorithms that can decode nervous systems activity, and a good understanding of the role touch and proprioception play in human self-awareness, artificial touch systems might become as common a technology as touch screen computers are today. 

References:

[1] Drewing, K. and Ernst, M.O.   Integration of force and position cues for shape perception through active touch. Brain Research, 1078, 92–100 (2006).

[1a] For some interesting examples, please visit the Jeka Lab at University of Maryland-College Park and the Multisensory Perception and Action group at Bielefeld University.

[2] Kiemel, T., Oie, K.S., and Jeka, J.J.   Multisensory fusion and the stochastic structure of postural sway.

Biological Cybernetics, 87, 262-277 (2002).

[2a] For examples of multisensory integration in the SC, please see: Stein, B.E. and Meredith, M.A.   The Merging of the Senses. MIT Press, Cambridge, MA (1993). 

For an example of multisensory integration in the PPC, please see: Pasalar, S., Ro, T., and Beauchamp, M.S.   TMS of posterior parietal cortex disrupts visual tactile multisensory integration. European Journal of Neuroscience, 31(10):1783-1790 (2010).

[3] Li, L., Rutlin, M., Abraira, V.E., Cassidy, C., Kus, L., Gong, S., Jankowski, M.P., Luo, W., Heintz, N., Koerber, H.R., Woodbury, C.J., and Ginty, D.D.   The Functional Organization of Cutaneous Low-Threshold Mechanosensory Neurons. Cell, 147, 1615–1627 (2011).

[4] Duenas, J., Chapuis, D., Pfeiffer, C., Martuzzi, R., Ionta, S., Blanke, O., and Gassert, R.   Neuroscience robotics to investigate multisensory integration and bodily awareness. Proceedings of the IEEE Engineering and Medicine in Biology Society, 8348-8352 (2011).

[4a] For more information, please see: Ernst, M.O. and Banks, M.S.   Humans integrate visual and haptic information in a statistically optimal fashion. Nature, 415, 429-433 (2002).

[4b] For an outline of this idea (with experiments!) please see: Alicea, B.  Performance Augmentation in Hybrid Systems: techniques and experiment. arXiv, 0810. 4629 [q-bio.NC, q-bio.QM] (2008). 

[5] Mate, C.W. and Carpick, R.W.   A sense for touch. Nature, 480, 189-190.

[5a] For reflections on the use of hierarchical material scaffolds to realize multiscalar material design, please see: Cranford, S.W. and Buehler, M.J.   Shaky foundations of hierarchical biological materials. Nano Today, 6, 332-338 (2011).

[6] Quake, S.R and Scherer, A.   From Micro- to Nanofabrication with Soft Materials. Science, 290, 1536-1540 (2000).

[7] Gao, H., Wang, X., Yao, H., Gorb, S., and Arzt, E. (2005). Mechanics of hierarchical adhesion structures of geckos. Mechanics of Materials, 37, 275-285.

[8] Wandersman, E., Candelier, R., Debregeas, G.,  and Prevost, A.   Texture-Induced Modulations of Friction Force: The Fingerprint Effect. Physical Review Letters, 107, 164301 (2011).

[9] Dixon, S.J., Collop, A.C., and Batt, M.E. (2000). Surface effects on ground reaction forces and lower extremity kinematics in running. Medicine and Science in Sports and Exercise, 32(11), 1919-1926.

[10] Lipomi, D.J., Vosgueritchian, M., Tee, B.C-K., Hellstrom, S.L., Lee, J.A., Fox, C.H., and Bao, Z.   Skin-like pressure and strain sensors based on transparent elastic films of carbon nanotubes. Nature Nanotechnology, (2012).

[11] Ying, M., Bonifas, A.P., Lu, N., Su, Y., Li, R., Cheng, H., Ameen, A., Huang, Y., and Rogers, J.A.   Silicon nanomembranes for fingertip electronics. Nanotechnology, 23, 344004 (2012).

[12] Alicea, B.   Nano-enabled Biological Materials. Nature Precedings, npre.2010.5448.1 (2010).

[13] Kim, D-H., Ghaffari, R., Lu, N., and Rogers, J.A.   Flexible and Stretchable Electronics for Biointegrated Devices. Annual Review of Biomedical Engineering, 14, 113-128 (2012).

The Rogers lab has come up with a number of interesting advanced applications in the area of confomal electronics, including wearable (tattooable) transistors and dissolvable devices (implantable that dissolve harmlessly once no longer needed) For more information on this application, please see:

Hwang, S-W., Tao, H., Kim, D-H., Cheng, H., Song, J-K., Rill, E., Brenckle, M.A., Panilaitis, B., Won, S.M., Kim, Y-S., Song, Y.M., Yu, K.J., Ameen, A., Li, R., Su, Y., Yang, M., Kaplan, D.L., Zakin, M.R., Slepian, M.J., Huang, Y., Omenetto, F.G., and Rogers, J.A.   A Physically Transient Form of Silicon Electronics. Science, 337, 1640 (2012).

Dissolvable thin film transistor partially immersed in solvent. COURTESY: iMedicalApps.com.

[14] Mannsfeld, S.C.B., Tee, B.C-K., Stoltenberg, R.M., Chen, C.V.H-H., Barman, S., Muir, B.V.O., Sokolov, A.N., Reese, C., and Bao, Z.   Highly sensitive flexible pressure sensors with microstructured rubber dielectric layers. Nature Materials, 9(9), 1-6 (2010).

[15] Slominski, A.T., Zmijewski, M.A., Skobowiat, C., Zbytek, B., Slominski, R.M., and Steketee, J.D. (2012). Sensing the environment: regulation of local and global homeostasis by the skin's neuroendocrine system. Advances in Anatomy, Embryology, and Cell Biology, 212, 1-115.

On Rats (cardiomyocytes) and Jellyfish (bodies)

Here is a recent Nature Biotechnology paper from the researchers at the Wyss Institute (Harvard) and the Dabiri Lab (Caltech) entitled "A tissue-engineered jellyfish with biomimetic propulsion" [1]. The authors of this paper reverse-engineered the essential mechanisms of a muscular pump to create an "artificial" form of jellyfish (Aurelia sp.) called a medusoid [2]. A medusoid (see Figure 1) consists of only a stripped-down version of the jellyfish morphology, replicating only the components needed to approximate jellyfish swimming kinematics [3].

Figure 1. Two examples of a free-swimming medusoid in solution. COURTESY: YouTube video [2].

Once these kinematics were understood, neonatal rat cardiomyocytes [4] were allowed to self-assemble into the desired structure. Cardiomyocytes will spontanously contract in culture, which enabled a cell population to approximate a nerve net. How did they do it? In this post, we will superficially step through the design process and show how the functional morphology of an organism can be engineered. Figure 2 shows the design process.

Figure 1. Steps in the Medusoid design process. COURTESY: Figure 1 (top) in [1].

The first step was abstract design principles from observed jellyfish propulsion. This biomimetic appraoch revealed that motor neurons, striated muscles, and radially-symmetrical appendages are primarily responsible for production of the stroke cycle [5]. The propulsion stroke in Aurelia is produced by two things: a radially symmetric and complete (e.g. power and recovery phases) "bell" contraction [6], and the synchronous activity of a distributed set of pacemakers [7]. In addition, muscle fibers in the jellyfish propulsion mechanism were found to be aligned end-to-end, which provides a mechanism for power production. Once these features were understood, the cellular architecture of the muscles and limbs were mapped using a chemical staining technique. This allowed for millimeter-scale organisms to be created. Morphogenesis was guided using structural (extracellular matrix scaffolding) and chemical (microenvironmental) cues, the results of which can be seen in Figure 3.

Figure 3. Results from the design and bioengineering efforts featured in [1]. COURTESY: Figure 1 (bottom) in [1].

To produce a medusoid body, cardiomyocytes were grown on a PDMS (polymer) scaffold. Because of this, there were constraints in terms of morphological compliance (e.g. bending capacity) [8], which is essential for the organism to initiate and complete its stroke. In the jellyfish, cells assemble around a material called mesoglea, which is a soft substrate supported by stiff ribs. This allows for selective rigidity and the signature bell-shaped contraction (see Figure 4 for comparison of contraction dynamics between Aurelia and the engineered organism).

Figure 4. Comparisons of kinematic performance between the jellyfish and medusoid. COURTESY: Figure 2 in [1].

To solve this design constraint, a lobed design was used. This balances stress generation by a cardiomyocyte population with the bending capacity of the substrate. Since reproducing a stroke-related movement identical to a jellyfish was not possible, a movement that involved a quasi-closed bell being formed at maximal contraction was used instead. These kinematics allowed for muscle fibers to be aligned with respect to the main axis of deformation, which allowed both stress production and substrate bending to be simultaneously maximized.

Figure 5. Evaluating the morphology of jellyfish and medusoids using a vortex flow field. COURTESY: Figure 3 in [1].

Finally, fluid-body interactions were characterized in order to fully optimize the medusoid morphology. These interactions are summarized in Figure 5. According to the authors of this study, the method presented here can be used to design any generalized biomechanical pump. Due to the use of cardiomyocytes, there is no ability to produce multi-stage movement behaviors [9]. However, the use of heterogeneous skeletal muscle fiber populations or transgenic muscle fibers engineered with respect to control of contraction speed may allow for more complicated movement behaviors to be reproduced. It will be interesting to see what types of "hybrid" species (part soft robot, part animal) these and other researchers are able to engineer in the future.

NOTES:

[1] Nawroth, J.C., Lee, H., Feinberg, A.W., Ripplinger, C.M., McCain, M.L., Grosberg, A., Dabiri, J.O., and Parker, K.K.   A tissue-engineered jellyfish with biomimetic propulsion. Nature Biotechnology, 30(8), 792-797 (2012).

[2] YouTube video of "Artificial jellyfish made from rat heart", Nature News. Full article at Nature News.

[3] a strategy similar to that used for designing the PETMAN robot from Boston Dynamics (see picture below). YouTube video here.

[4] for use of this cell type as an experimental model, please see: Chlopcikova, S., Psotova, J.,and Miketova, P.   Neonatal Rat Cardiomyocytes: a model for the study of morphological, biochemical, and electrophysiological characteristics of the heart. Biomedical Papers, 145(2), 49–55 (2001).

Picture of rat cardiomyocytes stained for tropomyosin. COURTESY: Lonza website.

[5] For information on a thermodynamic cycle, please see this. For information on swimming stroke (in humans), please see this.

[6] a "bell" contraction (where all appendages expand outward in the shape of a bell during muscle contraction) can be seen in the far left-hand panel of Figure 1.

[7] For information on cardiac pacemakers, please see this. For in silico simulation of pacemaker neuron dynamics, please see this tutorial from AnimatLab.

Example of a pacemaker cell from the SA node in the human heart. COURTESY: University of Utah Genetic Science Learning Center.

[8] For more information on how compliant substrates are used in soft robotics, please see: Trivedi, D., Rahn, C.D., Kier, W.M., and Walker, I.D.   Soft robotics: Biological inspiration, state of the art, and future research. Applied Bionics and Biomechanics, 5(3), 99–117 (2008).

[9] While these type of movements (e.g. associated with feeding or fighting) may require a central nervous system, they could be approximated using a jellyfish-like nerve net model. For more information on multi-stage movements, please see: Tanji, J.   Sequential Organization of Multiple Movements: involvement of cortical motor areas. Annual Review of Neuroscience, 24, 631–651 (2001).

Thingiverse, a treasure trove

In previous Synthetic Daisies posts, I have discussed the Maker movement and how you can engage in some pretty high-end technological innovation without too much overhead (see "Frontiers of Rapid Prototyping" and "Open Source Hardware" for more information). In the spirit of this theme, I am featuring a profile of Thingiverse, which is a repository of blueprints for objects and tools you can fabricate using a rapid prototyping machine.

Some of these objects are trivial, and others are quasi-useful. I will give a quick tour of different schematics available to download from Thingiverse, and then discuss how they can be used by the budding Maker.

Thing #1: MC Escher Cookie Maker

Do you like your cookies the same size and shape every time? Do you also like to serve them in a recursive manner? This cookie press might help on both counts. 

Thing #2: Che3po Chess

Ah, this is more my speed. Chess with liberal references to a post-rise-of-Skynet world and leetspeak. 

Thing #3: T800 Terminator Skull

If you indeed are interested in recreating a post-rise-of-Skynet world, here is a replica of a T800 terminator head (what lies beneath the skin, of course).

Thing #4: Hand robot InMoov

If you need to give a robot (or cyborg) a hand, here's your chance.

Thing #5: Bender Bending Rodriguez

Ah, yes, another robot. This one is a whole-body model, and in fact is the most famous Bending unit from Futurama. 

You might be asking at this point: can we make anything else besides robot parts and cookie cutters? In fact, there are thousands of designs available for download (although there is a heavy skew towards mechanical structures and simple tools). 

Of course, all of the above designs were "printed" using a rapid prototyper and a variety of raw materials. But suppose you do not have access to a rapid prototyper. Is Thingiverse still useful? Yes, it can be. All of the models are actually exchanged between users as a series of objects written in .STL (standard tesselation language) format. An example from "Che3po Chess" is shown in the image below:

The .STL format is not only accessible by software drivers for rapid prototyping machines. The models are build in an open-source program called MeshLab, which is good for mesh editing. Below is an example of the crown bishop from the "Che3po Chess" project opened in MeshLab.

Thingiverse could become quite useful in the design of virtual worlds, especially in mixed reality environments where physical objects and virtual objects co-exist in the same context. I am of course editorializing here, but by all means you should check out and experiment with Thingiverse.

The "nature" of materials: evolution and biomimetics

How do highly specialized biological materials evolve? An even better question is how the many different materials that make up animal bodies have come to coexist in the same organism. In this post, I will address the basics of these questions, although there is much to learn. This has applications to both basic research on biological systems and engineering methodology [1].

I will review the evolution of materials from three perspectives: the formation of biological composites in evolution, the phenomenon of layering in evolution, and the effects of evolving new structures on materials. Based on contemporary scientific findings, these are the most likely scientific mechanisms that account for the evolution of specialized materials and surfaces.

I. Biological composites
If you examine any segment of an animal body, you will find that it is composed of many different types of material. A human forearm, for example, is composed of fat layers, skeletal muscle, lamellar bone, and various other liquids and solids. This is a veritable kaleidoscope of tissue types, from a highly mineralized matrix (bone) to loosely-associated cell populations (fat layers). This diversity arises from the maintenance of two key mechanisms at the organ level: cell differentiation and tissue microenvironments. By contrast, biomechanical function acts to constrain the types of materials that can form through the forces experienced in functional contexts.

MRI image of human leg (left), highlighting the composite nature of the limb [2]. Material properties of trabecular bone (right) -- Voelcker Lab, Flinders University, Australia.

Cell differentiation. The differentiation of cells plays a role in the formation of these composites. In embryonic development, cell differentiation is partially determined its niche, or who its neighbors are. One possible organizing mechanism involves intercellular signaling molecules. This flexibility might allow for a wide range of materials to be formed in response to stresses and other cellular functions. It has been shown that cells can exhibit gene expression and protein production changes in response to the frictions induced by adhesion in vitro [3]. The stability of specific cell types might focus on the ability of these cells to absorb environmental stresses and fluctuations, which includes mechanical forces during movement and other interactions with the environment.

Tissue microenvironments. The aggregation of cells into tissues is also required for composite formation. More specifically, it is the co-existence of these cell populations in communities that allow for these composites to become well-integrated [4-6]. Cell populations residing in organs and other structures are organized in a manner analogous to an ecosystem, with energy exchange and substrate formation being prime candidates for the maintenance of homeostasis. Therefore, there is a hierarchical dependence leading from protein synthesis by individual cells to organismal context and back again that determine what materials will be formed in response to environmental and natural selective pressures.

Biomechanical function. While it seems counterintuitive, many structures that exist in nature may not be optimized for biomechanical function. Those that are “optimal” in terms of function tend to be highly specialized structures [7], and are also likely to be made from highly unique materials. Those structures that are less specialized in terms of function, or perform multiple functions simultaneously, should be made out of materials with a higher tribological diversity. Ultimately, these are testable predictions, but can also be inferred through examining the role of layering and the evolution of downstream [8] morphological structures.

II. Layering
In fields such as BioMEMS and bionanotechnology, a central issue is how very small functional devices can be fabricated. Generally, there are two methods for fabrication in very small devices: etching features into an existing surface, and deposition of materials onto an existing surface.

Examples of etching (left, courtesy London Centre for Nanotechnology) and deposition (right, courtesy ASME). Several research groups have used X-ray beams to etch patterns into very small surfaces (on the order of uM). Carbon nanotubes can be grown on a surface using a process called vapor deposition to modify very small surface function (on the order of uM).

Natural Microfabrication. In systems that are driven by natural processes, microfabrication cannot be top-down as engineering techniques generally are. A bottom-up strategy involves a mechanism called directed self-assembly [9]. In self-assembly, the configuration of a molecular system is biased by the available free energy, and the result is a highly-ordered system. The directed component comes into play in the form of "templates" or building blocks that guide further self-organization [10]. This is similar to the idea of building blocks in genetic algorithms, which appear to play a role in allowing for evolvable genotypes in silico.

One link between surfaces and materials fabricated through natural means and contemporary biomimetic engineering is the characterization of superhydrophobic surfaces. Hydrophobicity occurs when water molecules are repelled from a membrane rather than being absorbed by it. This is a feature characterized in nature by the lotus leaf, and is a design consideration in a range of BioMEMS applications.

Superhydrophobic surfaces are created by "dual-scale roughness". As the name implies, the surface exhibits a rough topology at two distinct spatial scales [11]. This further implies that hierarchical structures, with each component performing either a distinct or overlapping role, is required for evolving such surfaces. Surface stiffness is also a factor in guiding self-assembly [12], and may play the role of templates discussed in the previous section.

A picture characterizing the dual-scale roughness of a lotus leaf (courtesy, Soft Matter Interface group, Max Planck Institute).

Response to Function. While natural selection generally acts upon the entire organism, there may also be selective processes acting at multiple spatial scales within morphological structures. The structure of the Gecko's foot is an example of this. Like the lotus leaf, the Gecko's foot uses a hierarchical structure of grooves and cilia to maintain a highly specialized function [13-15]. This type of specialization is seen across plant and animal species as a diversity of biological attachment mechanisms.

While the "optimality of structure" idea presented as an outcome related to the biomechanical function of biological composites, is best exemplified by these systems, the existence of tribological diversity requires a different set of examples. To do this, we must turn to the evolution of a generalized trait, preferably one that plays a role in the biomechanics of an organism.

III. Evolution of the Jaw
In the evolution of the jaw, it appears that one change gives rise to another. The jaw evolved rather early in vertebrate phylogeny, constituting a group called Gnathostomes [16] and includes a diverse collection of forms. In mammals, the jaw allows for the mandible to articulate relative to the upper portion of the head in concert with muscle activity allows for chewing and active manipulation at the mouth opening. The range of motion in a jaw is variable, from the very large aperture of the hippopotamus to the more constrained mouth opening of a Primate.

Highly-stylized phylogenetic relationship between agnathans (e.g. lamprey, left) and gnathostomes (e.g. alligator snapping turtle and hippopotamus, center and right). Above phylogeny are the anatomical substrates of the jaw joint in non-eutherian Gnathostomes (left) and eutherian Gnathostomes (right).

Diagram showing the route from a joint (human temporomandibular joint, left) that can potentially transfer and/or dampen forces with regard to "downstream" morphological structures (right).

The evolution of a jaw has several indirect consequences, one of which is the introduction of large forces and stresses at the head. Much like in the case of vertebrate limbs, which are formed from highly durable and selective compliant [17] composite materials, the introduction of new functions requires a displacement of forces encountered during function.

A single evolutionary origin (monophyly). In the case of specialized and structurally specialized materials, such as specific instances of mineralized tissue, materials will arise once in a common ancestor and then be retained among members of a single clade. For example, vertebrates have tended to keep their skeletons made of either cartilage or hard bone. Major innovations in bone types tend to be restricted to specific clades. In cartilagenous fishes, the large-scale use of cartilage in the skeleton results in a single tissue type with the ability to endure a greater range of mechanical deformations. In mammals, hard bone comes in a number of forms (e.g. cortical, cancellous, and lamellar bone), each with their own physical properties and ability to endure and respond to various stresses and strains.

Multiple routes to refinement. The other option, observed in the origin of compounds such as chitin, is that a precursor material will evolve first and then be modified in various lineages to perform specific roles in a morphological system. For example, the basic chitin molecule may be adapted to a create a number of specialized materials in different lineages. Likewise, a basic set of molecules can be configured into different topologies through layering and/or other self-organized structures to produce highly-specialized materials. This is true of spider silk, which is used to build webs and other structures essential to their survival. Spider silk is a secreted protein that when spun into a silk strand has impressive mechanical properties. However, the performance characteristics of the resulting silk vary greatly in terms of both species of spider and gland of origin.

Conclusion
While the tribological profile of a given organisms is both determined by and a determiner of the evolution trajectory of a species, this can be approached from two perspectives. Reductionists will likely focus on the molecular building blocks of specific materials, answering questions such as: what are the signals that initiate the production of highly specific proteins and signaling molecules? Meanwhile, systems-level scientists will be more interested in the process of material synthesis during development, and answer questions such as: how is the self-assembly of highly specialized coordinated by generic processes? Both perspectives will be needed to fully appreciate the role specialized materials observed from across the diversity of the natural world and apply their artificial analogues to engineering technologies.

References and Notes

[1] Xia, F. and Jiang, L. (2008). Bio-inspired smart, multiscale interfacial materials. Advanced Materials, 20, 2842-2858.

[2] Courtesy: Imiaos.

[3] Mahoney, T.S. et.al (2001). Cell adhesion regulates gene expression at translational checkpoints in human myeloid leukocytes. PNAS USA, 98(18), 10284–10289.

[4] Poole, C.A. (1997). Articular cartilage chondrons: form, function and failure. Journal of Anatomy, 191, 1-13.

[5] Jeanes, A.I. et.al (2010). Cellular Microenvironment Influences the Ability of Mammary Epithelia to Undergo Cell Cycle. PLoS One, 6(3), e18144.

[6] Burdick, J.A. and Vunjak-Novakovic, G. (2009). Engineered Microenvironments for Controlled Stem Cell Differentiation. Tissue Engineering Part A, 15(2), 205-219.

[7] McNeill-Alexander, R. (1988). Elastic Mechanisms in Animal Movement. Cambridge University Press, Cambridge, UK.

[8] "downstream" in this case means structures whose change in function have an indirect effect on other structures.

[9] Romano, F. and Sciortino, F. (2011). Colloidal self-assembly: Patchy from the bottom up. Nature Materials 10, 171–173.

[10] Wang, D. and Mohwald, H. (2004). Template-directed colloidal self-assembly – the route to ‘top-down’ nanochemical engineering. Journal of Materials Chemistry, 14, 459-468.

[11] Shirtcliffe, N.J. et.al (2004). Dual-scale roughness produces unusually water-repellent surfaces. Advanced Materials, 16, 1929-1932.

[12] Kima, T.W. and Bhushan, B. (2007). Effect of stiffness of multi-level hierarchical attachment system on adhesion enhancement. Ultramicroscopy, 107, 10-11, 902-912.

[13] Gorb, S. and Scherge, M. (2000). Biological microtribology: anisotropy in frictional forces of orthopteran attachment pads reflects the ultrastructure of a highly deformable material. Proceedings of the Royal Society of London B, 267, 1239-1244.

[14] Arzt, E., Gorb, S., and Spolenak, R. (2003). From micro to nano contacts in biological attachment devices. PNAS, 100(19), 10603-10606.

[15] I refer interested readers to a comprehensive online bibliography covering research on the biology and engineering of surface adhesion and attachment mechanisms (Gecko-centric) hosted by the Robotics and Intelligent Machines Lab at the University of California-Berkeley.

[16] Tree of Life, Gnathostomes.

[17] flexible and pliable in response to functional needs. For example, bone (e.g. mineralized tissue) can be both rigid and flexible, depending on how it is loaded and degree of hysteretic response. Material compliance is not directly related to plasticity, although there may be some interesting parallels between the two phenomena.