Brook O. Swanson

The stomatopod dactyl club: a formidable damage-tolerant biological hammer.

Hammering Home the Lesson Stomatopods are marine crustaceans that use hammerlike claws for defense and to attack their prey. The claws undergo repeated high-velocity and high-force impacts. Weaver et al. (p. 1275; see the Perspective by Tanner) used a variety of techniques to examine the structure, mechanical behavior, and toughening mechanisms of the claw of the Peacock Mantis shrimp. The claws composite structure is optimized for toughness, which helps to prevent the complete failure that might arise from the claws repetitive hammering. The structure of mantis clubs is optimized to prevent complete failure caused by repetitive impacts. Nature has evolved efficient strategies to synthesize complex mineralized structures that exhibit exceptional damage tolerance. One such example is found in the hypermineralized hammer-like dactyl clubs of the stomatopods, a group of highly aggressive marine crustaceans. The dactyl clubs from one species, Odontodactylus scyllarus, exhibit an impressive set of characteristics adapted for surviving high-velocity impacts on the heavily mineralized prey on which they feed. Consisting of a multiphase composite of oriented crystalline hydroxyapatite and amorphous calcium phosphate and carbonate, in conjunction with a highly expanded helicoidal organization of the fibrillar chitinous organic matrix, these structures display several effective lines of defense against catastrophic failure during repetitive high-energy loading events.

TROPHIC POLYMORPHISM AND BEHAVIORAL DIFFERENCES DECREASE INTRASPECIFIC COMPETITION IN A CICHLID, HERICHTHYS MINCKLEYI

Resource polymorphisms, or morphological variations related to resource use, are common in fishes and are thought to be a possible step in speciation. This study experimentally tests the hypothesis that fitness (as estimated by growth rates) is increased by the presence of multiple trophic morphotypes (or morphs) within a population. Cage experiments were used to quantify the intraspecific competitive interactions between morphs of the polymorphic cichlid Herichthys minckleyi in Cuatro Cienegas, Mexico. Results sug- gest that competition is reduced between morphs in mixed-morph treatments relative to equal-density single-morph treatments. Field studies revealed that the morphs feed in dif- ferent microhabitats and use different feeding behaviors within these microhabitats. These results suggest that the polymorphism is maintained in the population because it decreases competition between the morphs, and that differences in feeding behavior facilitate resource partitioning.

SPIDER DRAGLINE SILK: CORRELATED AND MOSAIC EVOLUTION IN HIGH-PERFORMANCE BIOLOGICAL MATERIALS

Abstract The evolution of biological materials is a critical, yet poorly understood, component in the generation of biodiversity. For example, the diversification of spiders is correlated with evolutionary changes in the way they use silk, and the material properties of these fibers, such as strength, toughness, extensibility, and stiffness, have profound effects on ecological function. Here, we examine the evolution of the material properties of dragline silk across a phylogenetically diverse sample of species in the Araneomorphae (true spiders). The silks we studied are generally stronger than other biological materials and tougher than most biological or man-made fibers, but their material properties are highly variable; for example, strength and toughness vary more than fourfold among the 21 species we investigated. Furthermore, associations between different properties are complex. Some traits, such as strength and extensibility, seem to evolve independently and show no evidence of correlation or trade-off across species, even though trade-offs between these properties are observed within species. Material properties retain different levels of phylogenetic signal, suggesting that traits such as extensibility and toughness may be subject to different types or intensities of selection in several spider lineages. The picture that emerges is complex, with a mosaic pattern of trait evolution producing a diverse set of materials across spider species. These results show that the properties of biological materials are the target of selection, and that these changes can produce evolutionarily and ecologically important diversity.

The evolution of complex biomaterial performance: The case of spider silk.

Spider silk is a high-performance biomaterial with exceptional mechanical properties and over half a century of research into its mechanics, structure, and biology. Recent research demonstrates that it is a highly variable class of materials that differs across species and individuals in complex and interesting ways. Here, we review recent literature on mechanical variation and evolution in spider silk. We then present new data on material properties of silk from nine species of spiders in the Mesothelae and Mygalomorphae, the two basal clades of spiders. Silk from spiders in the Araneomorphae (true spiders where most previous research on silk has focused) is significantly stronger and therefore much tougher than the silk produced by spiders in the basal groups. These data support the hypothesis that the success and diversity seen in araneomorph spiders is associated with the evolution of this high-performance fiber. This comparative approach shows promise as a way to understand complex, high-performance biomaterials.

Biomaterials: Properties, variation and evolution

This is an energizing time to be a biomaterials scientist and an appropriate moment to examine the state-of-the-art, current trends and future directions in biomaterials research. In nearly every area of mathematics, physics, and engineering, there is a movement toward using biology as a source of interesting questions. In addition, the tools available for materials research have progressed to where they can be usefully applied to the complex problems at the heart of biological systems. It is clear from our symposium not only that biology is reaping the benefits of this collaboration, but that there is reciprocal illumination when biology provides new systems, directions, and techniques that drive related fields forward. In this short introduction to the symposium, we will highlight some of the trends that are emerging and point out some of the larger lessons that can be drawn from the examples that were presented. To adapt Otto Schmitt’s opinion of biophysics, a symposium on biomaterials is less a focus on a single discipline than a celebration of a point of view (Harkness 2002). The studies here are odd bedfellows: they share little in terms of individual technique, focal taxon, or ecofunctional niche. However, they all take advantage of the synergy at the interface between the materials sciences and biology. Fields as disparate as surface chemistry, biology, and materials science converge in their interest in biomaterials; unfortunately, researchers in one discipline are often not aware of, or informed about, the techniques and perspectives of another. We feel this has largely been a problem of insufficient contact between different disciplines and also the (necessarily) restrictive scopes of most research programs. Investigations have focused on either proximate (e.g., nanostructural and microstructural relationships with material properties) or ultimate questions (e.g., ecological and evolutionary impacts of material variation), with the connecting flows of information inadequate to unify the levels into a broader examination of performance. We are excited to present this symposium at a time when disciplinary divisions are blurring and biomaterials researchers of strikingly different backgrounds are working toward common ends and languages. The volume of biomaterial data is reaching new critical masses, for instance, allowing us to compare material stiffnesses across tissues, from nacre to bone to cartilage, and physical science tools (such as testing techniques for nanomaterials and Finite Element Analysis) are increasingly accessible to comparative biologists. Evolutionary biologists and physiologists are collaborating with engineers and computer scientists to study skeletal stresses in biting and running, deformations in wings and fins, and gripping in toes and tails. The scales of investigation spanned by these collaborations and the ever-increasing resolution of testing and imaging techniques stretch the scope of possible questions from genetics and protein interactions up through material and organismal performance and evolution. Modern biomaterials science, then, is a flavor of systems biology—a holistic approach to examining the functions and interactions of natural materials at multiple scales and from the perspectives of multiple disciplines. It is our hope that the assemblage of topics, presented in the contexts of organismal biology and evolution, will help to broaden the often mechanistic viewpoint of materials science and promote physical science approaches to biology.

Comparison of Embiopteran Silks Reveals Tensile and Structural Similarities across Taxa

Embioptera is a little studied order of widely distributed, but rarely seen, insects. Members of this group, also called embiids or webspinners, all heavily rely on silken tunnels in which they live and reproduce. However, embiids vary in their substrate preferences and these differences may result in divergent silk mechanical properties. Here, we present diameter measurements, tensile tests, and protein secondary structural analyses of silks spun by several embiid species. Despite their diverse habitats and phylogenetic relationships, these species have remarkably similar silk diameters and ultimate stress values. Yet, ultimate strain, Youngs modulus, and toughness vary considerably. To better understand these tensile properties, Fourier transformed infrared spectroscopy was used to quantify secondary structural components. Compared to other arthropod silks, embiid silks are shown to have consistent secondary structures, suggesting that commonality of amino acid sequence motifs and small differences in structural composition can lead to significant changes in tensile properties.

Functional mechanics of beetle mandibles: Honest signaling in a sexually selected system

Male stag beetles possess colossal mandibles, which they wield in combat to obtain access to females. As with many other sexually selected weapons, males with longer mandibles win more fights. However, variation in the functional morphology of these structures, used in male-male combat, is less well understood. In this study, mandible bite force, gape, structural strength, and potential tradeoffs are examined across a wide size range for one species of stag beetle, Cyclommatus metallifer. We found that not only does male mandible size demonstrate steep positive allometry, but the shape, relative bite force, relative gape, and safety factor of the mandibles also change with male size. Allometry in these functionally important mandibular traits suggests that larger males with larger mandibles should be better fighters, and that the mandibles can be considered an honest signal of male fighting ability. However, negative allometry in mandible structural safety factor, wing size, and flight muscle mass suggest significant costs and a possible limit on the size of the mandibles. J. Exp. Zool. 325A:3-12, 2016.

Parental care in the Cuatro Ciénegas cichlid, Herichthys minckleyi (Teleostei: Cichlidae)

Behavioral studies have often examined parental care by measuring phenotypic plasticity of behavior within a species. Phylogenetic studies have compared parental care among species, but only at broad categories (e.g., care vs. no care). Here we provide a detailed account that integrates phylogenetic analysis with quantitative behavioral data to better understand parental care behavior in the Cuatro Ciénegas cichlid, Herichthys minckleyi. We found that H. minckleyi occurs in a clade of sexually monochromatic or weakly dichromatic monogamous species, but that male and female H. minckleyi have dramatically different reproductive coloration patterns, likely as a result of sexual selection. Furthermore, we found that males are polygynous; large males guard large territories, and smaller males may attempt alternative mating tactics (sneaking). Finally, compared to the closely related monogamous Rio Grande cichlid, H. cyanoguttatus, males of H. minckleyi were present at their nests less often and performed lower rates of aggressive offspring defense, and females compensated for the absence of their mates by performing higher levels of offspring defense. Body color, mating system, and parental care in H. minckleyi appear to have evolved after it colonized Cuatro Ciénegas, and are likely a result of evolution in an isolated, stable environment.

Variation in foraging behavior facilitates resource partitioning in a polymorphic cichlid, Herichthys minckleyi

We examined foraging behavior (microhabitat use and feeding behavior) in a trophically polymorphic cichlid fish, Herichthys minckleyi, to address several questions regarding resource partitioning in this threatened species. These include: (1) do morphotypes demonstrate different foraging behaviors? (2) do individuals within a morphotype vary in their foraging behavior (e.g. are some individuals specialists, only using a subset of available resources, while other are generalists)? (3) do foraging behaviors vary between isolated pools? (4) do foraging behaviors vary across seasons? We quantified microhabitat use and feeding behavior for over 100 individuals (of two morphotypes) feeding freely in two isolated pools (populations) and across two seasons (winter and summer). We found differences in foraging behavior between morphotypes and individual specializations within morphotypes; i.e. some individuals specialize on certain food resources by using a few feeding behaviors within a subset of microhabitats, whereas others employ a range feeding behaviors across many microhabitats. Foraging behavior also varied between pools and across seasons. This spatial and temporal variation in foraging behavior and resource use may serve to maintain this polymorphism, as the relative fitness of the each morph may vary over space and time.

Do movement patterns differ between laboratory and field suction feeding behaviors in a Mexican cichlid

SynopsisWe analyzed feeding behavior of individuals of Herichthys minckleyi, the Cuatro Ciénegas cichlid, under laboratory conditions and freely behaving in their natural environment using high-speed video imaging. In a multivariate analysis of suction feeding behaviors there was no clear grouping of feeding events based on the environment, which suggests that most of the variability in the data was unrelated to differences between lab and field behaviors. In fact, the variability within an environment was far greater than the variability between the two environments. These results suggest that laboratory studies can accurately describe the kinematics of behaviors seen in the field. However, although lab based studies can quantify behaviors seen in the field, natural habitats are complex and provide individuals with the opportunity to exploit a wide range of food types and microhabitats, which may elicit behaviors not observed in the laboratory. However, feeding behaviors observed in the lab are representative of frequently used feeding behaviors in the field, at least for this species. Thus, we suggest that laboratory studies of feeding behavior, particularly those that test biomechanical or performance-based hypotheses can be extrapolated to natural environments.