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Ecomorphology is the study of relationships between organismal morphology and ecology. As such, it is the only way to determine if morphometric data can be used as an informative proxy for ecological variables of interest. To achieve this goal, ecomorphology often depends on, or directly tests, assumptions about the nature of the relationships among morphology, performance, and ecology. We discuss three approaches to the study of ecomorphology: morphometry-driven, function-driven, and ecology-driven and study design choices inherent to each approach. We also identify 10 assumptions that underlie ecomorphological research: 4 of these are central to all ecomorphological studies and the remaining 6 are variably applicable to some of the specific approaches described above. We discuss how these assumptions may impact ecomorphological studies and affect the interpretation of their findings. We also point out some limitations of ecomorphological studies, and highlight some ways by which we can strengthen, validate, or eliminate systematic assumptions.

 

Integration is an essential feature of complex biomechanical systems, with coordination and covariation occurring among and within structural components at time scales that vary from microseconds to deep evolutionary time. Integration has been suggested to both promote and constrain morphological evolution, and the effects of integration on the evolution of structure likely vary by system, clade, historical contingency, and time scale. In this introduction to the 2019 symposium “Multifunctional Structures and Multistructural Functions,” we discuss the role of integration among structures in the context of functional integration and multifunctionality. We highlight articles from this issue of Integrative and Comparative Biology that explore integration within and among kinematics, sensory and motor systems, physiological systems, developmental processes, morphometric dimensions, and biomechanical functions. From these myriad examples it is clear that integration can exist at multiple levels of organization that can interact with adjacent levels to result in complex patterns of structural and functional phenotypes. We conclude with a synthesis of major themes and potential future directions, particularly with respect to using multifunctionality, itself, as a trait in evolutionary analyses.

 

Newly-developed methods for utilizing performance surfaces—multivariate representations of the relationship between phenotype and functional performance—allow researchers to test hypotheses about adaptive landscapes and evolutionary diversification with explicit attention to functional factors. Here, information from performance surfaces of three turtle shell functions—shell strength, hydrodynamics, and self-righting—is used to test the hypothesis that turtle lineages transitioning from aquatic to terrestrial habitats show patterns of shell shape evolution consistent with decreased importance of hydrodynamic performance. Turtle shells are excellent model systems for evolutionary functional analysis. The evolution of terrestriality is an interesting test case for the efficacy of these methods because terrestrial turtles do not show a straightforward pattern of morphological convergence in shell shape: many terrestrial lineages show increased shell height, typically assumed to decrease hydrodynamic performance, but there are also several lineages where the evolution of terrestriality was accompanied by shell flattening. Performance surface analyses allow exploration of these complex patterns and explicit quantitative analysis of the functional implications of changes in shell shape. Ten lineages were examined. Nearly all terrestrial lineages, including those which experienced decreased shell height, are associated with morphological changes consistent with a decrease in the importance of shell hydrodynamics. This implies a common selective pattern across lineages showing divergent morphological patterns. Performance studies such as these hold great potential for integrating adaptive and performance data in macroevolutionary studies.

 

Terrestrial animals move in complex habitats that vary over space and time. The characteristics of these habitats are not only defined by the physical environment, but also by the photic environment, even though the latter has largely been overlooked. For example, numerous studies of have examined the role of habitat structure, such as incline, perch diameter, and compliance, on running performance. However, running performance likely depends heavily on light level. Geckos are an exceptional group for analyzing the role of the photic environment on locomotion as they exhibit several independent shifts to diurnality from a nocturnal ancestor, they are visually-guided predators, and they are extremely diverse. Our initial goal is to discuss the range of photic environments that can be encountered in terrestrial habitats, such as day versus night, canopy cover in a forest, fog, and clouds. We then review the physiological optics of gecko vision with some new information about retina structures, the role of vision in motor-driven behaviors, and what is known about gecko locomotion under different light conditions, before demonstrating the effect of light levels on gecko locomotor performance. Overall, we highlight the importance of integrating sensory and motor information and establish a conceptual framework as guide for future research. Several future directions, such as understanding the role of pupil dynamics, are dependent on an integrative framework. This general framework can be extended to any motor system that relies on sensory information, and can be used to explore the impact of performance features on diversification and evolution.

 

Many species have evolved alternate phenotypes, thus enabling individuals to conditionally produce phenotypes that are favorable for reproductive success. Examples of this phenomenon include sexual dimorphism, alternative reproductive strategies, and social insect castes. While the evolutionary functions and developmental mechanisms of dimorphic phenotypes have been studied extensively, little attention has focused on the evolutionary covariance between each phenotype. We extend the conceptual framework and methods of morphological integration to hypothesize that dimorphic traits tend to be less integrated between sexes or social castes. In the case of social insects, we describe results from our recent study of an ant genus in which workers have major and minor worker castes that perform different behavioral repertoires in and around the nest. In the case of birds, we describe a new analysis of a family of songbirds that exhibits plumage coloration that can differ greatly between males and females, with apparently independent changes in each sex. Ant head shape, which is highly specialized in each worker caste, was weakly integrated between worker castes, whereas thorax shape, which is more monomorphic, was tightly integrated. Similarly, in birds, we found a negative association between dimorphism and the degree of integration between sexes. We also found that integration decreased in fairy wrens (Malurus) for many feather patches that evolved greater dichromatism. Together, this suggests that the process of evolving increased dimorphism results in a decrease in integration between sexes and social castes. We speculate that once a mechanism for dimorphism evolves, that mechanism can create independent variation in one sex or caste upon which selection may act.

 

Organisms are composed of hierarchically arranged component parts that must work together to successfully achieve whole organism functions. In addition to integration among individual parts, some ecological demands require functional systems to work together in a type of inter-system performance integration. While performance can be measured by the ability to successfully accomplish ecologically relevant tasks, integration across performance traits can provide a deeper understanding of how these traits allow an organism to survive. The ability to move and the ability to consume food are essential to life, but during prey capture these two functions are typically integrated. Suction-feeding fishes have been used as a model of these interactions, but it is unclear how other ecologically relevant scenarios might reduce or change integration. To stimulate further research into these ideas, we highlight three contexts with the potential to result in changes in integration and underlying performance traits: (1) behavioral flexibility in aquatic feeding modes for capturing alternative prey types, (2) changes in the physical demands imposed by prey capture across environments, and (3) secondary adaptation for suction prey capture behaviors. These examples provide a broad scope of potential drivers of integration that are relevant to selection pressures experienced across vertebrate evolution. To demonstrate how these ideas can be applied and stimulate hypotheses, we provide observations from preliminary analyses of locally adapted populations of Trinidadian guppies (Poecilia reticulata) capturing prey using suction and biting feeding strategies and an Atlantic mudskipper (Periophthalmus barbarus) capturing prey above and below water. We also include a re-analysis of published data from two species of secondarily aquatic cetaceans, beluga whales (Delphinapterus leucas) and Pacific white-sided dolphins (Lagenorhynchus obliquidens), to examine the potential for secondary adaptation to affect integration in suction prey capture behaviors. Each of these examples support the broad importance of integration between locomotor and feeding performance but outline new ways that these relationships can be important when suction demands are reduced or altered. Future work in these areas will yield promising insights into vertebrate evolution and we hope to encourage further discussion on possible avenues of research on functional integration during prey capture.

 

Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems.

 

Complex structures, like the vertebrate skull, are composed of numerous elements or traits that must develop and evolve in a coordinated manner to achieve multiple functions. The strength of association among phenotypic traits (i.e., integration), and their organization into highly-correlated, semi-independent subunits termed modules, is a result of the pleiotropic and genetic correlations that generate traits. As such, patterns of integration and modularity are thought to be key factors constraining or facilitating the evolution of phenotypic disparity by influencing the patterns of variation upon which selection can act. It is often hypothesized that selection can reshape patterns of integration, parceling single structures into multiple modules or merging ancestrally semi-independent traits into a strongly correlated unit. However, evolutionary shifts in patterns of trait integration are seldom assessed in a unified quantitative framework. Here, we quantify patterns of evolutionary integration among regions of the archosaur skull to investigate whether patterns of cranial integration are conserved or variable across this diverse group. Using high-dimensional geometric morphometric data from 3D surface scans and computed tomography scans of modern birds (n = 352), fossil non-avian dinosaurs (n = 27), and modern and fossil mesoeucrocodylians (n = 38), we demonstrate that some aspects of cranial integration are conserved across these taxonomic groups, despite their major differences in cranial form, function, and development. All three groups are highly modular and consistently exhibit high integration within the occipital region. However, there are also substantial divergences in correlation patterns. Birds uniquely exhibit high correlation between the pterygoid and quadrate, components of the cranial kinesis apparatus, whereas the non-avian dinosaur quadrate is more closely associated with the jugal and quadratojugal. Mesoeucrocodylians exhibit a slightly more integrated facial skeleton overall than the other grades. Overall, patterns of trait integration are shown to be stable among archosaurs, which is surprising given the cranial diversity exhibited by the clade. At the same time, evolutionary innovations such as cranial kinesis that reorganize the structure and function of complex traits can result in modifications of trait correlations and modularity.

 

Abstract Convergent evolution is at the forefront of many form-function studies. There are many examples of multiple independent lineages evolving a similar morphology in response to similar functional demands, providing a framework for testing hypotheses of form-function evolution. However, there are numerous clades with underappreciated convergence, in which there is a perceived homogeneity in morphology. In these groups, it can be difficult to investigate causal relationships of form and function (e.g., diet influencing the evolution of jaw morphology) without the ability to disentangle phylogenetic signal from convergence. Leuciscids (Cypriniformes: Leuciscidae; formerly nested within Cyprinidae) are a species-rich clade of fishes that have diversified to occupy nearly every freshwater trophic niche, yet are considered to have relatively low morphological diversity relative to other large freshwater clades. Within the North American leuciscids, many genera contain at least one herbivore, insectivore, and larvaphage. We created 3D models from micro-computed tomography scans of 165 leuciscid species to measure functionally relevant traits within the pharyngeal jaws of these fishes. Using a published phylogeny, we tested these metrics for evolutionary integration, phylogenetic signal, and correlation with diet. Measurements of the pharyngeal jaws, muscle attachment areas, and teeth showed strong positive evolutionary correlation with each other and negative evolutionary correlation with measurements of the inter-ceratobranchial ligament (ICB ligament). Using diet data from published literature, we found extensive dietary convergence within Leuciscidae. The most common transitions we found were between herbivorous and invertivorous taxa and between insectivore types (aquatic vs. terrestrial). We document a trade-off in which herbivorous leuciscids have large teeth, short ICB ligaments, and large muscle attachment areas, whereas insectivorous leuciscids showed the opposite pattern. Inverse patterns of morphological integration between the ICB ligament the rest of the pharyngeal jaw correspond this dietary trade-off, which indicates that coordinated evolution of morphological traits contributes to functional diversity in this clade. However, these patterns only emerge in the context of phylogeny, meaning that the pharyngeal jaws of North American leuciscids converge by similar means (structural changes in response to dietary demands), but not necessarily to similar ends (absolute phenotype). 

Abstract While functional morphologists have long studied the evolution of anatomical structures, the origin of morphological novelties has received less attention. When such novelties first originate they must become incorporated into an integrated system to be rendered fully functional. Thus, developmental integration is key at the origin of morphological novelties. However, given enough evolutionary time such integration may be broken, allowing for a division of labor that is facilitated by subsequent decoupling of structures. Cypriniformes represent a diverse group of freshwater fishes characterized by several trophic novelties that include: kinethmoid-mediated premaxillary protrusion, a muscular palatal and post-lingual organ, hypertrophied lower pharyngeal jaws that masticate against the base of the neurocranium, novel pharyngeal musculature controlling movement of the hypertrophied lower pharyngeal jaws, and in a few species an incredibly complex epibranchial organ used to aggregate filtered phytoplankton. Here, we use the wealth of such trophic novelties in different cypriniform fishes to present case studies in which developmental integration allowed for the origin of morphological innovations. As proposed in case studies 1 and 2 trophic innovations may be associated with both morphological and lineage diversification. Alternatively, case studies 3 and 4 represent a situation where ecological niche was expanded but with no concomitant increase in species diversity.