Calcium carbonate skeletons of scleractinian corals amplify light availability to their algal symbionts by diffuse scattering, optimizing photosynthetic energy acquisition. However, the mechanism of ...scattering and its role in coral evolution and dissolution of algal symbioses during "bleaching" events are largely unknown. Here we show that differences in skeletal fractal architecture at nano/micro-lengthscales within 96 coral taxa result in an 8-fold variation in light-scattering and considerably alter the algal light environment. We identified a continuum of properties that fall between two extremes: (1) corals with low skeletal fractality that are efficient at transporting and redistributing light throughout the colony with low scatter but are at higher risk of bleaching and (2) corals with high skeletal fractality that are inefficient at transporting and redistributing light with high scatter and are at lower risk of bleaching. While levels of excess light derived from the coral skeleton is similar in both groups, the low-scatter corals have a higher rate of light-amplification increase when symbiont concentration is reduced during bleaching, thus creating a positive feedback-loop between symbiont concentration and light-amplification that exposes the remaining symbionts to increasingly higher light intensities. By placing our findings in an evolutionary framework, in conjunction with a novel empirical index of coral bleaching susceptibility, we find significant correlations between bleaching susceptibility and light-scattering despite rich homoplasy in both characters; suggesting that the cost of enhancing light-amplification to the algae is revealed in decreased resilience of the partnership to stress.
Damselfishes (Perciformes, Pomacentridae) are a major component of coral reef communities, and the functional diversity of their trophic anatomy is an important constituent of the ecological ...morphology of these systems. Using shape analyses, biomechanical modelling, and phylogenetically based comparative methods, we examined the anatomy of damselfish feeding among all genera and trophic groups. Coordinate based shape analyses of anatomical landmarks were used to describe patterns of morphological diversity and determine positions of functional groups in a skull morphospace. These landmarks define the lever and linkage structures of the damselfish feeding system, and biomechanical analyses of this data were performed using the software program JawsModel4 in order to calculate the simple mechanical advantage (MA) employed by different skull elements during feeding, and to compute kinematic transmission coefficients (KT) that describe the efficiency with which angular motion is transferred through the complex linkages of damselfish skulls.
Our results indicate that pomacentrid planktivores are significantly different from other damselfishes, that biting MA values and protrusion KT ratios are correlated with pomacentrid trophic groups more tightly than KT scores associated with maxillary rotation and gape angle, and that the MAs employed by their three biting muscles have evolved independently. Most of the biomechanical parameters examined have experienced low levels of phylogenetic constraint, which suggests that they have evolved quickly.
Joint morphological and biomechanical analyses of the same anatomical data provided two reciprocally illuminating arrays of information. Both analyses showed that the evolution of planktivory has involved important changes in pomacentrid functional morphology, and that the mechanics of upper jaw kinesis have been of great importance to the evolution of damselfish feeding. Our data support a tight and biomechanically defined link between structure and the functional ecology of fish skulls, and indicate that certain mechanisms for transmitting motion through their jaw linkages may require particular anatomical configurations, a conclusion that contravenes the concept of "many-to-one mapping" for fish jaw mechanics. Damselfish trophic evolution is characterized by rapid and repeated shifts between a small number of eco-morphological states, an evolutionary pattern that we describe as reticulate adaptive radiation.
Biological color may be adaptive or incidental, seasonal or permanent, species- or population-specific, or modified for breeding, defense or camouflage. Although color is a hugely informative aspect ...of biology, quantitative color comparisons are notoriously difficult. Color comparison is limited by categorization methods, with available tools requiring either subjective classifications, or expensive equipment, software, and expertise. We present an R package for processing images of organisms (or other objects) in order to quantify color profiles, gather color trait data, and compare color palettes on the basis of color similarity and amount. The package treats image pixels as 3D coordinates in a "color space," producing a multidimensional color histogram for each image. Pairwise distances between histograms are computed using earth mover's distance, a technique borrowed from computer vision, that compares histograms using transportation costs. Users choose a color space, parameters for generating color histograms, and a pairwise comparison method to produce a color distance matrix for a set of images. The package is intended as a more rigorous alternative to subjective, manual digital image analyses, not as a replacement for more advanced techniques that rely on detailed spectrophotometry methods unavailable to many users. Here, we outline the basic functions of colordistance, provide guidelines for the available color spaces and quantification methods, and compare this toolkit with other available methods. The tools presented for quantitative color analysis may be applied to a broad range of questions in biology and other disciplines.
The evolution of feeding mechanisms in the ray-finned fishes (Actinopterygii) is a compelling example of transformation in a musculoskeletal complex involving multiple skeletal elements and numerous ...muscles that power skull motion. Biomechanical models of jaw force and skull kinetics aid our understanding of these complex systems and enable broad comparison of feeding mechanics across taxa. Mechanical models characterize how muscles move skeletal elements by pulling bones around points of rotation in lever mechanisms, or by transmitting force through skeletal elements connected in a linkage. Previous work has focused on the feeding biomechanics of several lineages of fishes, but a broader survey of skull function in the context of quantitative models has not been attempted. This study begins such a survey by examining the diversity of mechanical design of the oral jaws in 35 species of ray-finned fishes with three main objectives: (1) analyze lower jaw lever models in a broad phylogenetic range of taxa, (2) identify the origin and evolutionary patterns of change in the linkage systems that power maxillary rotation and upper jaw protrusion, and (3) analyze patterns of change in feeding design in the context of actinopterygian phylogeny. The mandibular lever is present in virtually all actinopterygians, and the diversity in lower jaw closing force transmission capacity, with mechanical advantage ranging from 0.04 to 0.68, has important functional consequences. A four-bar linkage for maxillary rotation arose in the Amiiformes and persists in various forms in many teleost species. Novel mechanisms for upper jaw protrusion based on this linkage for maxillary rotation have evolved independently at least five times in teleosts. The widespread anterior jaws linkage for jaw protrusion in percomorph fishes arose initially in Zeiformes and subsequently radiated into a wide range of premaxillary protrusion capabilities.
The family Labridae (including scarines and odacines) contains 82 genera and about 600 species of fishes that inhabit coastal and continental shelf waters in tropical and temperate oceans throughout ...the world. The Labridae (the wrasses) is the fifth largest fish family and second largest marine fish family, and is one of the most morphologically and ecologically diversified families of fishes in size, shape, and color. Labrid phylogeny is a long-standing problem in ichthyology that is part of the larger question of relationships within the suborder Labroidei. A phylogenetic analysis of labrids was conducted to investigate relationships among the six classical tribes of wrasses, the affinities of the wrasses to the parrotfishes (scarines), and the broad phylogenetic structure among labrid genera. Four gene fragments were sequenced from 98 fish species, including 84 labrid fishes and 14 outgroup taxa. Taxa were chosen from all major labrid clades and most major global ocean regions where labrid fishes exist, as well as cichlid, pomacentrid, and embiotocid outgroups. From the mitochondrial genome we sequenced portions of 12S rRNA (1000
bp) and 16S rRNA (585
bp), which were aligned by using a secondary structure model. From the nuclear genome, we sequenced part of the protein-coding genes RAG2 (846
bp) and Tmo4C4 (541
bp). Maximum likelihood, maximum parsimony, and Bayesian analyses on the resulting 2972
bp of DNA sequence produced similar topologies that confirm the monophyly of a family Labridae that includes the parrotfishes and butterfishes and strong support for many previously identified taxonomic subgroups. The tribe Hypsigenyini (hogfishes, tuskfishes) is the sister group to the remaining labrids and includes odacines and the chisel-tooth wrasse
Pseudodax moluccanus, a species previously considered close to scarines. Cheilines and scarines are sister-groups, closely related to the temperate Labrini, and pseudocheilines and cheilines are split in all phylogenies. The razorfishes (novaculines) and temperate pseudolabrines form successive sister clades to the large crown group radiation of the Julidini. The cleaner wrasses (Labrichthyini) are nested within this radiation and several julidine genera do not appear to be monophyletic (e.g.,
Coris and
Halichoeres). Invasion of temperate water by this predominantly tropical group has occurred multiple times and the reconstruction of biogeography assuming an Indo-Pacific ancestor results in five different lineages invading the Atlantic/Caribbean region. Functional novelties in the feeding apparatus have allowed labrid fishes to occupy nearly every feeding guild in reef environments, and trophic variation is a central axis of diversification in this family.
Abstract
Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes ...by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. 3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.
The reefs surrounding the Gilbert Islands (Republic of Kiribati, Central Pacific), like many throughout the world, have undergone a period of rapid and intensive environmental perturbation over the ...past 100 years. A byproduct of this perturbation has been a reduction of the number of shark species present in their waters, even though sharks play an important in the economy and culture of the Gilbertese. Here we examine how shark communities changed over time periods that predate the written record in order to understand the magnitude of ecosystem changes in the Central Pacific. Using a novel data source, the shark tooth weapons of the Gilbertese Islanders housed in natural history museums, we show that two species of shark, the Spot-tail (Carcharhinus sorrah) and the Dusky (C. obscurus), were present in the islands during the last half of the 19(th) century but not reported in any historical literature or contemporary ichthyological surveys of the region. Given the importance of these species to the ecology of the Gilbert Island reefs and to the culture of the Gilbertese people, documenting these shifts in baseline fauna represents an important step toward restoring the vivid splendor of both ecological and cultural diversity.
Fish skulls are complex kinetic systems with movable components that are powered by muscles. Cranial muscles for jaw closing pull the mandible around a point of rotation at the jaw joint using a ...third-order lever mechanism. The present study develops a lever model for the jaw of fishes that uses muscle design and the Hill equation for nonlinear length–tension properties of muscle to calculate dynamic power output. The model uses morphometric data on skeletal dimensions and muscle proportions in order to predict behavior and force transmission mediated by lever action. The computer model calculates a range of dynamic parameters of jaw function including muscle force, torque, effective mechanical advantage, jaw velocity, bite duration, bite force, work and power. A complete list of required morphometrics is presented and a software program (MandibLever 2.0) is available for implementing lever analysis. Results show that simulations yield kinematics and timing profiles similar to actual fish feeding events. Simulation of muscle properties shows that mandibles reach their peak velocity near the start of jaw closing, peak force at the end of jaw closing, and peak power output at about 25% of the closing cycle time. Adductor jaw muscles with different mechanical designs must have different contractile properties and/or different muscle activity patterns to coordinate jaw closing. The effective mechanical advantage calculated by the model is considerably lower than the mechanical advantage estimated from morphological lever ratios, suggesting that previous studies of morphological lever ratios have overestimated force and underestimated velocity transmission to the mandible. A biomechanical model of jaw closing can be used to interpret the mechanics of a wide range of jaw mechanisms and will enable studies of the functional results of developmental and evolutionary changes in skull morphology and physiology.
The biomechanics of animal limbs has evolved to meet the functional demands for movement associated with different behaviors and environments. Effective movement relies not only on limb mechanics but ...also on appropriate mechanosensory feedback. By comparing sensory ability and mechanics within a phylogenetic framework, we show that peripheral mechanosensation has evolved with limb biomechanics, evolutionarily tuning the neuromechanical system to its functional demands. We examined sensory physiology and mechanics of the pectoral fins, forelimb homologs, in the fish family Labridae. Labrid fishes exhibit extraordinary morphological and behavioral diversity and use pectoral fin-based propulsion with fins ranging in shape from high aspect ratio (AR) wing-like fins to low AR paddle-like fins. Phylogenetic character analysis demonstrates that high AR fins evolved independently multiple times in this group. Four pairs of species were examined; each included a plesiomorphic low AR and a high AR species. Within each species pair, the high AR species demonstrated significantly stiffer fin rays in comparison with the low AR species. Afferent sensory nerve activity was recorded during fin ray bending. In all cases, afferents of stiffer fins were more sensitive at lower displacement amplitudes, demonstrating mechanosensory tuning to fin mechanics and a consistent pattern of correlated evolution. We suggest that these data provide a clear example of parallel evolution in a complex neuromechanical system, with a strong link between multiple phenotypic characters: pectoral fin shape, swimming behavior, fin ray stiffness, and mechanosensory sensitivity.
Summary
Quantitative, three‐dimensional measurements of anatomy in biology and paleontology are key to understanding the evolutionary processes underlying morphological, functional and ecological ...diversification. However, the collection of 3D morphometric data from a large number of samples or in the field is currently limited by methods that are either too costly, too time‐consuming or lack portability.
We present a new R package, StereoMorph, for the rapid and accurate collection of 3D landmarks and curves using two standard digital cameras. StereoMorph provides a complete set of tools for every step in the collection of 3D landmarks and curves using a stereo camera set‐up. This includes image processing and optimization functions for automated camera calibration using a checkerboard pattern, an easy‐to‐use application for digitizing landmarks and curves from photographs, and tools for reconstructing points and curves in 3D. The image processing tools and digitizing application are readily applicable to 2D morphometrics as well, enabling 2D landmarks and curves to be digitized and scaled automatically using a checkerboard pattern.
We include five examples that demonstrate key functionalities of StereoMorph: automated detection of checkerboard corners, camera calibration, testing calibration accuracy, digitizing photographs and 3D curve reconstruction. With a set‐up costing less than $1500, we show that it is possible to achieve a mean reconstruction error of less than 30 microns. Once the cameras are assembled, specimens can be photographed as quickly as with 2D morphometrics while digitizing takes two to three times as long as digitizing a single photograph.
We conclude by presenting an accompanying tutorial which details all of the steps required to collect 3D landmarks and curves using StereoMorph. Additionally, we present a web blog that will provide a platform for updates and user questions and suggestions.
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