An official website of the United States government
Abstract Adaptive radiations are striking examples of rapid speciation along ecological lines. In adaptive radiations, fast rates of lineage diversification often pair with rapid rates of morphological diversification. Such diversification has often been documented through the lens of ecological drivers, overlooking the intrinsic structural constraints that may also have a key role in configuring patterns of trait diversification. Covariation within and between traits has been hypothesized to govern the axes of trait evolution, either by increasing the degree of covariation between traits (i.e. integration), which promotes morphological coordination, or by strengthening the degree of covariation within traits (i.e. modularity), which allows organisms to explore novel trait combinations and different regions of morphospace. Here, we study the modularity of the skull within an adaptive radiation of pupfishes that is endemic to San Salvador Island, Bahamas. This radiation exhibits divergent craniofacial morphologies, including generalist, snail-eating specialist, and scale-eating specialist species. We assessed morphological disparity, integration strength, and modularity patterns across the sympatric San Salvador Island pupfish radiation, lab-reared hybrids, and closely related outgroup species. Our findings revealed an unexpected uniformity in the pattern of modularity across diverse species, supporting a five-module functional hypothesis comprising the oral jaw, pharyngeal jaw, neurocranium, hyoid apparatus, and hyomandibula. Despite this conserved modularity pattern, all species exhibited weak but significantly varying strengths of overall between-module integration and significant disparity across all cranial regions. Our results suggest rapid morphological diversification can occur even with conserved patterns of modularity. We propose that broadscale patterns of modularity are more conserved while between-module associations are more evolvable between species.
more »
« less
Morphological integration and cranial modularity in six genera of echimyid rodents (Rodentia: Echimyidae)
Abstract Rodents of the family Echimyidae present a wide variety of life histories and ecomorphological adaptations. This study evaluated morphological integration patterns, modularity, and evolutionary flexibility in six Echimyid genera representing ecomorphological extremes within the family. The relationships between traits were evaluated by comparing estimated covariance and correlations matrices of populations. The presence of modules was investigated by comparing the patterns of integration between traits and using hypothetical matrices based on shared development/function and masticatory stress. The results point to a common covariance and correlation pattern among the six echimyid genera, suggesting a conserved pattern of covariation (associations among traits) throughout the evolution of this group. The overall magnitude of integration, however, varied greatly. We also found a high degree of modularity in all six echimyid genera. Finally, we observed a clear association between flexibility, i.e., the ability of a species to respond to the direction of selection, with the overall magnitude of integration and degree of modularization. The results of this study provide hypotheses concerning the underlying effects of the association among traits, which may have facilitated or constrained the evolution of morphological variation in the diverse family Echimyidae.
more »
« less
- Award ID(s):
- 1754748
- PAR ID:
- 10325988
- Editor(s):
- Rowe, Kevin
- Date Published:
- Journal Name:
- Journal of Mammalogy
- ISSN:
- 0022-2372
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Quantifying and characterizing the pattern of trait covariances is crucial for understanding how population-level patterns of integration might constrain or facilitate craniofacial evolution related to the feeding system. This study addresses an important gap in our knowledge by investigating magnitudes and patterns of morphological integration of biomechanically informative traits in the skulls of Homo sapiens, Pan troglodytes, and Gorilla gorilla. We predicted a lower magnitude of integration among human biomechanical traits since humans eat a softer, less biomechanically challenging diet than apes. Indeed, compared to African apes, the magnitudes of integration were lower in H. sapiens skulls for form data (raw dimensions) but were similar or higher for shape data (raw dimensions scaled by geometric mean). Patterns of morphological integration were generally similar, but not identical, across the three species, particularly for the form data compared to the shape data. Traits that load heavily on the primary axis of variation in morphospace are generally associated with size and/or shape of the temporalis and masseter muscles and with dimensions related to the constrained lever model of jaw biomechanics. Given the conserved nature of morphological integration, skull adaptations for food processing in African apes and humans may have been constrained to occur along certain paths of high evolvability. The conserved pattern of functional integration also indicates that extant hominine species can operate as reasonable analogues for extinct hominins in studies that require population-level patterns of trait variance/covariance.more » « less
-
Abstract 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.more » « less
-
Abstract ObjectivesModular architecture of traits in complex organisms can be important for morphological evolution at micro‐ and sometimes macroevolutionary scales as it may influence the tempo and direction of changes to groups of traits that are essential for particular functions, including food acquisition and processing. We tested several distinct hypotheses about craniofacial modularity in the hominine skull in relation to feeding biomechanics. Materials and MethodsFirst, we formulated hypothesized functional modules for craniofacial traits reflecting specific demands of feeding biomechanics (e.g., masseter leverage/gape or tooth crown mechanics) inHomo sapiens,Pan troglodytes, andGorilla gorilla. Then, the pattern and strength of modular signal was quantified by the covariance ratio coefficient and compared across groups using covariance ratio effect size. Hierarchical clustering analysis was then conducted to examine whether a priori‐defined functional modules correspond to empirically recovered clusters. ResultsThere was statistical support for most a priori‐defined functional modules in the cranium and half of the functional modules in the mandible. Modularity signal was similar in the cranium and mandible, and across the three taxa. Despite a similar strength of modularity, the empirically recovered clusters do not map perfectly onto ourpriorifunctional modules, indicating that further work is needed to refine our hypothesized functional modules. ConclusionThe results suggest that modular structure of traits in association with feeding biomechanics were mostly shared with humans and the two African apes. Thus, conserved patterns of functional modularity may have facilitated evolutionary changes to the skull during human evolution.more » « less
-
Abstract The field of comparative morphology has entered a new phase with the rapid generation of high-resolution three-dimensional (3D) data. With freely available 3D data of thousands of species, methods for quantifying morphology that harness this rich phenotypic information are quickly emerging. Among these techniques, high-density geometric morphometric approaches provide a powerful and versatile framework to robustly characterize shape and phenotypic integration, the covariances among morphological traits. These methods are particularly useful for analyses of complex structures and across disparate taxa, which may share few landmarks of unambiguous homology. However, high-density geometric morphometrics also brings challenges, for example, with statistical, but not biological, covariances imposed by placement and sliding of semilandmarks and registration methods such as Procrustes superimposition. Here, we present simulations and case studies of high-density datasets for squamates, birds, and caecilians that exemplify the promise and challenges of high-dimensional analyses of phenotypic integration and modularity. We assess: (1) the relative merits of “big” high-density geometric morphometrics data over traditional shape data; (2) the impact of Procrustes superimposition on analyses of integration and modularity; and (3) differences in patterns of integration between analyses using high-density geometric morphometrics and those using discrete landmarks. We demonstrate that for many skull regions, 20–30 landmarks and/or semilandmarks are needed to accurately characterize their shape variation, and landmark-only analyses do a particularly poor job of capturing shape variation in vault and rostrum bones. Procrustes superimposition can mask modularity, especially when landmarks covary in parallel directions, but this effect decreases with more biologically complex covariance patterns. The directional effect of landmark variation on the position of the centroid affects recovery of covariance patterns more than landmark number does. Landmark-only and landmark-plus-sliding-semilandmark analyses of integration are generally congruent in overall pattern of integration, but landmark-only analyses tend to show higher integration between adjacent bones, especially when landmarks placed on the sutures between bones introduces a boundary bias. Allometry may be a stronger influence on patterns of integration in landmark-only analyses, which show stronger integration prior to removal of allometric effects compared to analyses including semilandmarks. High-density geometric morphometrics has its challenges and drawbacks, but our analyses of simulated and empirical datasets demonstrate that these potential issues are unlikely to obscure genuine biological signal. Rather, high-density geometric morphometric data exceed traditional landmark-based methods in characterization of morphology and allow more nuanced comparisons across disparate taxa. Combined with the rapid increases in 3D data availability, high-density morphometric approaches have immense potential to propel a new class of studies of comparative morphology and phenotypic integration.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/jmammal/gyab151
