Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes

Morphological diversification does not proceed evenly across the organism. Some body parts tend to evolve at higher rates than others, and these rate biases are often attributed to sexual and natural selection or to genetic constraints. We hypothesized that variation in the rates of morphological evolution among body parts could also be related to the performance consequences of the functional systems that make up the body. Specifically, we tested the widely held expectation that the rate of evolution for a trait is negatively correlated with the strength of biomechanical trade-offs to which it is exposed. We quantified the magnitude of trade-offs acting on the morphological components of three feeding-related functional systems in four radiations of teleost fishes. After accounting for differences in the rates of morphological evolution between radiations, we found that traits that contribute more to performance trade-offs tend to evolve more rapidly, contrary to the prediction. While ecological and genetic factors are known to have strong effects on rates of phenotypic evolution, this study highlights the role of the biomechanical architecture of functional systems in biasing the rates and direction of trait evolution.     

Particulate versus integrated evolution of the upper body in late pleistocene humans: A test of two models

Evolutionary biologists are largely polarized in their approaches to integrating microevolutionary and macroevolutionary processes. Neo-Darwinians typically seek to identify population-level selective and genetic processes that culminate in macroevolutionary events. Epigeneticists and structuralists, on the other hand, emphasize developmental constraints on the action of natural selection, and highlight the role of epigenetic shifts in producing evolutionary change in morphology. Accordingly, the ways in which these paradigms view and address morphological contrasts between classes of related organisms differ. These paradigms, although seldomly explicitly stated, emerge in paleoanthropology as well. Considerations of postcranial morphological contrasts between archaic and modern humans typically fall into one of two broad interpretive models. The first derives from the neo-Darwinian perspective and holds that evolution in the postcranial skeleton was largely mosaic (operating in a particulate manner), and that temporal change in specific traits informs us about behavioral shifts or genetic evolution affecting isolated anatomical regions (i.e., adaptive behavioral inferences can be made from comparative studies of individual trait complexes). The alternative model follows from the epigeneticist paradigm and sees change in specific postcranial traits as correlated responses to change in overall body form (involving shifts in regulation of skeletal growth, or selective and developmental responses to broad adaptive shifts). By this view, integration of functional systems both constrains and directs evolution of various traits, and morphological contrasts inform us about overall change in body form related to change in such things as overall growth patterns, climatic adaptation, and technological dependency. These models were tested by confirmatory factor analysis using measures of upper body form and upper limb morphological traits in Eurasian Neandertal and early modern fossils and recent human samples. Results indicate (1) a model of morphological integration fits the data better than a model of no integration, but (2) this integration accounts for less than half of the variance in upper limb traits, suggesting a high degree of tolerance for particulate evolution in the context of an integrated upper body plan. Significant relationships were detected between joint shapes and body size, between humeral shaft shape and body size and chest shape, and between measures of biomechanical efficiency and robusticity. The observed morphological differences between late archaic and early modern humans reflect particulate evolution in the context of constraints imposed by genetic and morphological integration. While particulate approaches to interpreting the fossil record appear to be justified, attention must also be paid to delineating the nature and extent of morphological integration and its role in both constraining and producing observed patterns of variation between groups. Confirmatory factor analysis provides a means of examining trait covariance matrices, and serves as a useful method of identifying patterns of integration in morphology. © 1996 Wiley-Liss, Inc.     

Genetics of body shape and armour variation in threespine sticklebacks

Patterns of genetic variation and covariation can influence the rate and direction of phenotypic evolution. We explored the possibility that the parallel morphological evolution seen in threespine stickleback (Gasterosteus aculeatus) populations colonizing freshwater environments is facilitated by patterns of genetic variation and covariation in the ancestral (marine) population. We estimated the genetic (G) and phenotypic (P) covariance matrices and directions of maximum additive genetic (g(max) ) and phenotypic (p(max) ) covariances of body shape and armour traits. Our results suggest a role for the ancestral G in explaining parallel morphological evolution in freshwater populations. We also found evidence of genetic constraints owing to the lack of variance in the ancestral G. Furthermore, strong genetic covariances and correlations among traits revealed that selective factors responsible for threespine stickleback body shape and armour divergence may be difficult to disentangle. The directions of g(max) and p(max) were correlated, but the correlations were not high enough to imply that phenotypic patterns of trait variation and covariation within populations are very informative of underlying genetic patterns.     

Brain evolution and development: adaptation,allometry and constraint

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.     

There's something afoot in the evolution of ontogenies

Allometry, the association between size and shape, has long been considered an evolutionary constraint because of its ability to channel variation in particular directions in response to evolution of size. Several recent studies, however, have demonstrated that allometries themselves can evolve. Therefore, constraints based on these allometries are not constant over long evolutionary time scales. The changes in ontogeny appear to have a clear adaptive basis, which establishes a feedback loop from adaptive change of ontogeny through the altered developmental constraints to the potential for further evolutionary change. Altogether, therefore, this new evidence underscores the tight interactions between developmental and ecological factors in the evolution of morphological traits.     

Early developmental plasticity and integrative responses in arctic charr (Salvelinus alpinus): effects of water velocity on body size and shape

Environmental conditions such as temperature and water velocity may induce changes among alternative developmental pathways, i.e. phenotypic responses, in vertebrates. However, the extent to which the environment induces developmental plasticity and integrated developmental responses during early ontogeny of fishes remains poorly documented. We analyzed the responses of newly hatched Arctic charr (Salvelinus alpinus) to four experimental water velocities during 100 days of development. To our knowledge, this work is the first to analyze developmental plasticity responses of body morphology to an experimental gradient of water velocities during early ontogeny of fish. Arctic charr body size and shape responses show first, that morphometric traits display significant differences between low and high water velocities, thus revealing directional changes in body traits. Secondly, trait variation allows the recognition of critical ontogenetic periods that are most responsive to environmental constraints (40-70 and 80-90 days) and exhibit different levels of developmental plasticity. This is supported by the observation of asynchronous timing of variation peaks among treatments. Third, morphological interaction of traits is developmentally plastic and time-dependent. We suggest that developmental responses of traits plasticity and interaction at critical ontogenetic periods are congruent with specific environmental conditions to maintain the functional integrity of the organism.     

Evolutionary persistence of phenotypic integration: influence of developmental and functional relationships on complex trait evolution

Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.     

Internal and external constraints in the evolution of morphological allometries in a butterfly

Much diversity in animal morphology results from variation in the relative size of morphological traits. The scaling relationships, or allometries, that describe relative trait size can vary greatly in both intercept and slope among species or other animal groups. Yet within such groups, individuals typically exhibit low variation in relative trait size. This pattern of high intra- and low intergroup variation may result from natural selection for particular allometries, from developmental constraints restricting differential growth among traits, or both. Here we explore the relative roles of short-term developmental constraints and natural selection in the evolution of the intercept of the allometry between the forewing and hindwing of a butterfly. First, despite a strong genetic correlation between these two traits, we show that artificial selection perpendicular to the forewing-hindwing scaling relationship results in rapid evolution of the allometry intercept. This demonstrates an absence of developmental constraints limiting intercept evolution for this scaling relationship. Mating experiments in a natural environment revealed strong stabilizing selection favoring males with the wild-type allometry intercept over those with derived intercepts. Our results demonstrate that evolution of this component of the forewing-hindwing allometry is not limited by developmental constraints in the short term and that natural selection on allometry intercepts can be powerful.     

Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies

Evolution can be viewed as a series of changes in the developmental program along the phylogenetic tree. To better understand the early evolution of the vertebrate skull, we can use the embryos of the cyclostome species as models. By comparing the cyclostome developmental patterns with those of gnathostomes, it becomes possible to distinguish the primitive and derived parts of the developmental program as taxon-specific traits. These traits are often recognizable as developmental constraints that define taxa by biasing the developmental trajectories within a certain limited range, resulting in morphological homologies in adults. These developmental constraints are distributed on the phylogenetic tree like the morphological character states of adult animals and are associated with specific regions of the tree. From this perspective, we emphasize the importance of considering gene expression and embryonic anatomy as the mechanistic bases that can result in homologous or nonhomologous morphological patterns at later developmental stages. Taking the acquisition of the jaw and trabecula cranii as examples, we demonstrate that a set of embryonic features can be coupled or decoupled during evolution and development. When they are coupled, they exert an ancestral developmental constraint that results in homologous morphological patterns, and when they are decoupled, the ancestral constraints tend to be abandoned, generating a new body plan. The heterotopy behind the specification of the oral domain is an example of decoupling, based on shifted tissue interactions. We also stress the importance of "developmental burden" in determining the sequential order of changes through evolution.     

MODELING PHENOTYPIC PLASTICITY IN GROWTH TRAJECTORIES: A STATISTICAL FRAMEWORK

Phenotypic plasticity, that is multiple phenotypes produced by a single genotype in response to environmental change, has been thought to play an important role in evolution and speciation. Historically, knowledge about phenotypic plasticity has resulted from the analysis of static traits measured at a single time point. New insight into the adaptive nature of plasticity can be gained by an understanding of how organisms alter their developmental processes in a range of environments. Recent advances in statistical modeling of functional data and developmental genetics allow us to construct a dynamic framework of plastic response in developmental form and pattern. Under this framework, development, genetics, and evolution can be synthesized through statistical bridges to better address how evolution results from phenotypic variation in the process of development via genetic alterations.     

QUANTITATIVE GENETICS OF SHAPE IN CRICKET WINGS: DEVELOPMENTAL INTEGRATION IN A FUNCTIONAL STRUCTURE

The role of developmental and genetic integration for evolution is contentious. One hypothesis states that integration acts as a constraint on evolution, whereas an alternative is that developmental and genetic systems evolve to match the functional modularity of organisms. This study examined a morphological structure, the cricket wing, where developmental and functional modules are discordant, making it possible to distinguish the two alternatives. Wing shape was characterized with geometric morphometrics, quantitative genetic information was extracted using a full‐sibling breeding design, and patterns of developmental integration were inferred from fluctuating asymmetry of wing shape. The patterns of genetic, phenotypic, and developmental integration were clearly similar, but not identical. Heritabilities for different shape variables varied widely, but no shape variables were devoid of genetic variation. Simulated selection for specific shape changes produced predicted responses with marked deflections due to the genetic covariance structure. Three hypotheses of modularity according to the wing structures involved in sound production were inconsistent with the genetic, phenotypic, or developmental covariance structure. Instead, there appears to be strong integration throughout the wing. The hypothesis that genetic and developmental integration evolve to match functional modularity can therefore be rejected for this example.     

The accumulation of reproductive isolation in early stages of divergence supports a role for sexual selection

Models of speciation by sexual selection propose that male–female coevolution leads to the rapid evolution of behavioural reproductive isolation. Here, we compare the strength of behavioural isolation to ecological isolation, gametic incompatibility and hybrid inviability in a group of dichromatic stream fishes. In addition, we examine whether any of these individual barriers, or a combined measure of total isolation, is predicted by body shape differences, male colour differences, environmental differences or genetic distance. Behavioural isolation reaches the highest values of any barrier and is significantly greater than ecological isolation. No individual reproductive barrier is associated with any of the predictor variables. However, marginally significant relationships between male colour and body shape differences with ecological and behavioural isolation are discussed. Differences in male colour and body shape predict total reproductive isolation between species; hierarchical partitioning of these two variables' effects suggests a stronger role for male colour differences. Together, these results suggest an important role for divergent sexual selection in darter speciation but raise new questions about the mechanisms of sexual selection at play and the role of male nuptial ornaments.     

Integration and modularity of teleostean pectoral fin shape and its role in the diversification of acanthomorph fishes

Phenotypic integration and modularity describe the strength and pattern of interdependencies between traits. Integration and modularity have been proposed to influence the trajectory of evolution, either acting as constraints or facilitators. Here, we examine trends in the integration and modularity of pectoral fin morphology in teleost fishes using geometric morphometrics. We compare the fin shapes of the highly diverse radiation of acanthomorph fishes to lower teleosts. Integration and modularity are measured using two‐block partial least squares analysis and the covariance ratio coefficient between the radial bones and lepidotrichia of the pectoral fins. We show that the fins of acanthomorph fishes are more tightly integrated but also more morphologically diverse and faster evolving compared to nonacanthomorph fishes. The main pattern of shape covariation in nonacanthomorphs is concordant with the main trajectory of evolution between nonacanthomorphs and acanthomorphs. Our findings support a facilitating role for integration during the acanthomorph diversification. Potential functional consequences and developmental mechanisms of fin integration are discussed.     

Phylogenetic perspectives on reef fish functional traits

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef‐associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid‐sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.     

The fish tail as a derivation from axial musculoskeletal anatomy: an integrative analysis of functional morphology

The adult morphology of the tail varies greatly among extant fishes despite sharing both ontogenetic similarities and the functional need to propel the body through a fluid medium. Both sharks (Chondrichthyes) and ray-finned fishes (Actinopterygii) control caudal fin musculature independently of axial body myomere activity to modify the stiffness and shape of their tails. For example, sharks and bony fishes possess different structural elements and muscles and move their tails in different ways, resulting in different locomotory hydrodynamic effects and a range of performance variables including speed and maneuverability. The stiffness of the heterocercal, lobate tail of the shark can be modulated during the tail beat resulting in nearly continuous thrust production. In contrast, the highly flexible tail of ray-finned fishes can be manipulated into many different shape conformations enabling increased maneuverability for these fishes. Consequently, the developmental, morphological, and functional derivation of the tail from the axial trunk has resulted in a diversity of form, the attributes of which may be of ecological and evolutionary significance.     

Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan‐tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time‐dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time‐dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.     

Morphological variation and covariation in mandibular molars of platyrrhine primates

Molars are highly integrated biological structures that have been used for inferring evolutionary relationships among taxa. However, parallel and convergent morphological traits can be affected by developmental and functional constraints. Here, we analyze molar shapes of platyrrhines in order to explore if platyrrhine molar diversity reflects homogeneous patterns of molar variation and covariation. We digitized 30 landmarks on mandibular first and second molars of 418 extant and 11 fossil platyrrhine specimens to determine the degree of integration of both molars when treated as a single module. We combined morphological and phylogenetic data to investigate the phylogenetic signal and to visualize the history of molar shape changes. All platyrrhine taxa show a common shape pattern suggesting that a relatively low degree of phenotypic variation is caused by convergent evolution, although molar shape carries significant phylogenetic signal. Atelidae and Pitheciidae show high levels of integration with low variation between the two molars, whereas the Cebinae/Saimiriinae, and especially Callitrichinae, show greater variation between molars and trend toward a modular organization. We hypothesize that biomechanical constraints of the masticatory apparatus, and the dietary profile of each taxon are the main factors that determine high covariation in molars. In contrast, low molar shape covariation may result from the fact that each molar exhibits a distinct ecological signal, as molars can be exposed to distinct occlusal loadings during food processing, suggesting that different selective pressures on molars can reduce overall molar integration.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

Evolution of body shape in differently coloured sympatric congeners and allopatric populations of Lake Malawi's rock‐dwelling cichlids

The cichlid fishes of Lake Malawi represent one of the most diverse adaptive radiations of vertebrates known. Among the rock‐dwelling cichlids (mbuna), closely related sympatric congeners possess similar trophic morphologies (i.e. cranial and jaw structures), defend overlapping or adjacent territories, but can be easily distinguished based on male nuptial coloration. The apparent morphological similarity of congeners, however, leads to an ecological conundrum: theory predicts that ecological competition should lead to competitive exclusion. Hence, we hypothesized that slight, yet significant, ecological differences accompanied the divergence in sexual signals and that the divergence of ecological and sexual traits is correlated. To evaluate this hypothesis, we quantified body shape, a trait of known ecological importance, in populations of Maylandia zebra, a barred, widespread mbuna, and several sympatric nonbarred congeners. We found that the barred populations differ in body shape from their nonbarred sympatric congeners and that the direction of shape differences was consistent across all barred vs. nonbarred comparisons. Barred populations are generally deeper bodied which may be an adaptation to the structurally complex habitat they prefer, whereas the nonbarred species have a more fusiform body shape, which may be adaptive in their more open microhabitat. Furthermore, M. zebra populations sympatric with nonbarred congeners differ from populations where the nonbarred phenotype is absent and occupy less morphospace, indicating potential ecological character displacement. Mitochondrial DNA as well as published AFLP data indicated that the nonbarred populations are not monophyletic and therefore may have evolved multiple times independently. Overall our data suggest that the evolution of coloration and body shape may be coupled as a result of correlational selection. We hypothesize that correlated evolution of sexually selected and ecological traits may have contributed to rapid speciation as well as the maintenance of diversity in one of the most diverse adaptive radiations known.