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
Specimen alignment with limited point-based homology: 3D morphometrics of disparate bivalve shells (Mollusca: Bivalvia)
Background Comparative morphology fundamentally relies on the orientation and alignment of specimens. In the era of geometric morphometrics, point-based homologies are commonly deployed to register specimens and their landmarks in a shared coordinate system. However, the number of point-based homologies commonly diminishes with increasing phylogenetic breadth. These situations invite alternative, often conflicting, approaches to alignment. The bivalve shell (Mollusca: Bivalvia) exemplifies a homologous structure with few universally homologous points—only one can be identified across the Class, the shell ‘beak’. Here, we develop an axis-based framework, grounded in the homology of shell features, to orient shells for landmark-based, comparative morphology. Methods Using 3D scans of species that span the disparity of shell morphology across the Class, multiple modes of scaling, translation, and rotation were applied to test for differences in shell shape. Point-based homologies were used to define body axes, which were then standardized to facilitate specimen alignment via rotation. Resulting alignments were compared using pairwise distances between specimen shapes as defined by surface semilandmarks. Results Analysis of 45 possible alignment schemes finds general conformity among the shape differences of ‘typical’ equilateral shells, but the shape differences among atypical shells can change considerably, particularly those with distinctive modes of growth. Each alignment corresponds to a hypothesis about the ecological, developmental, or evolutionary basis of morphological differences, but we suggest orientation via the hinge line for many analyses of shell shape across the Class, a formalization of the most common approach to morphometrics of shell form. This axis-based approach to aligning specimens facilitates the comparison of approximately continuous differences in shape among phylogenetically broad and morphologically disparate samples, not only within bivalves but across many other clades.
more »
« less
- Award ID(s):
- 1633535
- NSF-PAR ID:
- 10359591
- Date Published:
- Journal Name:
- PeerJ
- Volume:
- 10
- ISSN:
- 2167-8359
- Page Range / eLocation ID:
- e13617
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Synopsis Urbanization, despite its destructive effects on natural habitats, offers species an opportunity to colonize novel niches. Previous research found that urban Anolis lizards in Puerto Rico had increased adhesive toepad area and more ventral toepad scales, traits that are likely adaptive and genetically based. We further investigated these phenotypic changes using geometric morphometrics to measure differences in toe shape, toepad shape, and lamellar morphology. Our results indicate that the increased toepad area of urban Anolis cristatellus lizards in Puerto Rico is not simply an isometric increase in toe size. Toes of urban populations exhibit multiple disproportional changes compared to forest lizards, with a larger proportion of the toe length covered in adhesive toepad. In addition, the toepads of urban lizards increase more in length than width. Lastly, lizards in urban populations exhibit both increased number of lamellae as well as increased spacing between individual lamellae. We also observed regional variation, with urban specimens having significantly more disparity, suggesting similar processes of urban adaptation are likely happening in parallel across the island, yet with region-specific idiosyncrasies, possibly generating more variation in toepad morphology across urban specimens as compared to forest specimens. Considering the use of geometric morphometrics, we found that specimen preparation, specifically how flat and straight toes are during imaging, to be an important factor affecting our data, more so than specimen size or any other meaningful morphological variation. In addition, we found that landmark and semilandmark data can be used to directly estimate toepad area, offering the opportunity to streamline future studies. In conclusion, our results highlight the value of considering toepad morphology in more detail beyond adhesive pad area or number of lamellae. Geometric morphometrics tools may be employed to elucidate subtle differences in shape to better allow researchers to connect changes in morphology to ecology and adhesive performance.
-
Spiral ribs are among the most common morphological features in mollusk shells and previous studies have shown them to have functional significance with expected evolutionary consequences. Many previous studies, however, have treated these features as potentially analogous across taxa, without examining whether they may have important constructional dissimilarities. Mollusk shells are made of multiple layers of calcite or aragonite which may exhibit different microstructure or microstructure orientations which may in turn impact their mechanical properties. In this study, five specimens of marine mollusks with spiral ribs, including three turritellid gastropods and two bivalves, were examined under SEM to examine microstructure of ribbed region in comparison of non-ribbed region. SEM imaging revealed differences in the number and thickness of distinct microstructural layers of each shell and allowed comparisons to be made between the ribbed and non-ribbed region of each specimen, providing a greater understanding of how these ribs were constructed during shell deposition. Ribs in all specimens are formed through the thickening of single or multiple crossed-lamellar layers, but differences in rib ultrastructures were found among species and different ribs of same species, showing great diversity and complexity of constructional mechanisms. This diversity in rib construction might indicate heterology in the development of shell sculpture, especially mechanisms for differences in concurrently deposited rib strength. This is especially notable for turritellids where the pattern of onset of spiral ornamentation is phylogenetically informative, suggesting homology of rib identity. Further study will be conducted on turritellid gastropods in different lineages to explore the taxonomic meaning of different rib constructional mechanisms.more » « less
-
more » « less
ABSTRACT Mollusc and brachiopod shells have served as biological armour for hundreds of millions of years. Studying shell strength in compression experiments can provide insights into macroevolution, predator–prey dynamics, and anthropogenic impacts on aquatic ecosystems. These studies have been conducted across fields including palaeontology, ecology, conservation biology and engineering using a range of techniques for a variety of purposes. Using this approach, studies have demonstrated that predators can cause changes in prey shell morphology in the laboratory over both short timescales and over longer evolutionary timescales. Similarly, environmental factors such as nutrient concentration and ocean acidification have been shown to influence shell strength. Experimental compression tests have been used to study the functional morphology of shell‐crushing predators and to test how the taphonomic state of shells (e.g. presence of drill holes, degree of shell degradation) may influence their likelihood of being preserved in the fossil record. This review covers the basic principles and experimental design of compression tests used to infer shell strength. Although many investigations have used this methodology, few provide a detailed explanation of how meaningfully to interpret data generated using compression experiments for those unfamiliar with this method. Furthermore, this review provides a compilation of the findings of studies that have employed these experimental methods to address specific themes: taphonomy, morphology, predation, environmental variables, and climate change. Many authors have used experimental compression tests, however, disparities among methodologies (e.g. in experimental design, taxa, specimen preservation, etc.) limit the applicability of findings from taxon‐specific studies to broader eco‐evolutionary questions. The review highlights confounding factors, such as shell thickness, size, damage, microstructure, and taphonomic state, and address how they can be mitigated using three‐dimensional (3D)‐printed model shells. 3D prints have been demonstrated as valuable proxies for understanding aspects of shell morphology that cannot otherwise be experimentally isolated. Using 3D printed models allows simplification of complex biological systems for idealized experimental studies. Such studies can isolate specific aspects of shell morphology to establish fundamental relationships between form and function. Establishing standardized methods of testing shell strength in this way will not only permit comparison across studies but also will enable investigators systematically to add complexity to their models.
-
more » « less
Abstract The evolutionary history of archosaurs and their closest relatives is characterized by a wide diversity of locomotor modes, which has even been suggested as a pivotal aspect underlying the evolutionary success of dinosaurs vs. pseudosuchians across the Triassic–Jurassic transition. This locomotor diversity (e.g., more sprawling/erect; crouched/upright; quadrupedal/bipedal) led to several morphofunctional specializations of archosauriform limb bones that have been studied qualitatively as well as quantitatively through various linear morphometric studies. However, differences in locomotor habits have never been studied across the Triassic–Jurassic transition using 3D geometric morphometrics, which can relate how morphological features vary according to biological factors such as locomotor habit and body mass. Herein, we investigate morphological variation across a dataset of 72 femora from 36 different species of archosauriforms. First, we identify femoral head rotation, distal slope of the fourth trochanter, femoral curvature, and the angle between the lateral condyle and crista tibiofibularis as the main features varying between bipedal and quadrupedal taxa, all of these traits having a stronger locomotor signal than the lesser trochanter's proximal extent. We show a significant association between locomotor mode and phylogeny, but with the locomotor signal being stronger than the phylogenetic signal. This enables us to predict locomotor modes of some of the more ambiguous early archosauriforms without relying on the relationships between hindlimb and forelimb linear bone dimensions as in prior studies. Second, we highlight that the most important morphological variation is linked to the increase of body size, which impacts the width of the epiphyses and the roundness and proximodistal position of the fourth trochanter. Furthermore, we show that bipedal and quadrupedal archosauriforms have different allometric trajectories along the morphological variation in relation to body size. Finally, we demonstrate a covariation between locomotor mode and body size, with variations in femoral bowing (anteroposterior curvature) being more distinct among robust femora than gracile ones. We also identify a decoupling in fourth trochanter variation between locomotor mode (symmetrical to semi‐pendant) and body size (sharp to rounded). Our results indicate a similar level of morphological disparity linked to a clear convergence in femoral robusticity between the two clades of archosauriforms (Pseudosuchia and Avemetatarsalia), emphasizing the importance of accounting for body size when studying their evolutionary history, as well as when studying the functional morphology of appendicular features. Determining how early archosauriform skeletal features were impacted by locomotor habits and body size also enables us to discuss the potential homoplasy of some phylogenetic characters used previously in cladistic analyses as well as when bipedalism evolved in the avemetatarsalian lineage. This study illuminates how the evolution of femoral morphology in early archosauriforms was functionally constrained by locomotor habit and body size, which should aid ongoing discussions about the early evolution of dinosaurs and the nature of their evolutionary “success” over pseudosuchians.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7717/peerj.13617
