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The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

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Abstract

Significance Variation is the raw material for evolution, but studies have yet to unify the effects of intrinsic genetic and developmental interactions that influence variation with the extrinsic factors that shape organismal diversity on a large scale. Analysis of phenotypic integration can bridge different facets of evolutionary study and address fundamental questions on developmental and evolutionary dynamics through deep time. Our study of Late Pleistocene saber-toothed cats and dire wolves demonstrates that developmental integration channeled increasing amounts of morphological variation through 27,000 years of climate change, validating results from laboratory-based studies with the natural experiments captured in the fossil record.

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... Despite generally strong stabilizing selection on developmental outputs, interactions occurring during ontogeny across levels of organization-from gene regulation and cellular transduction to tissue formation and endocrine signalsinduce stochastic developmental variation, even in the absence of genetic or environmental perturbation [13,14]. Focusing on this intrinsic developmental stochasticity, we here take advantage of multivariate FA in trait shape to quantify developmental variability independent of environmental and genetic variation [15][16][17]. In bilaterally symmetric organisms, the left and the right side of the same individual share the exact same genotype and environment, yet, there are often slight differences between both sides that can be attributed to developmental interactions (after accounting for measurement error and directional asymmetry, and assuming somatic mutational effects are negligible, see [18]). ...
... These findings recapitulate patterns in other species where mutational covariation predicts evolutionary divergences across millions of years (e.g. [51]) and systems where developmental integration predicts phenotypic covariation among individuals [15][16][17]52]. Collectively, our results support the hypothesis that changes in horn shape-whether brought about by plastic responses to environmental change, functional genetic perturbations, or short and long-term evolutionary divergences-are biased by the developmental system underpinning horn shape. ...
... This is consistent with a major role of developmental variability (or bias) in shaping phenotypic variation, plasticity and evolutionary changes over considerable timespans. The finding that FA aligns with the effects of functional genetic manipulations suggests that FA, which has mostly been discussed in terms of developmental instability and integration [16,19], may be a useful tool to study the role of developmental bias in evolution. More broadly, our study adds to the growing literature suggesting that developmental architectures influence evolutionary dynamics. ...
Article
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The degree to which developmental systems bias the phenotypic effects of environmental and genetic variation, and how these biases affect evolution, is subject to much debate. Here, we assess whether developmental variability in beetle horn shape aligns with the phenotypic effects of plasticity and evolutionary divergence, yielding three salient results. First, we find that most pathways previously shown to regulate horn length also affect shape. Second, we find that the phenotypic effects of manipulating divergent developmental pathways are correlated with each other as well as multivariate fluctuating asymmetry-a measure of developmental variability. Third, these effects further aligned with thermal plasticity, population differences and macroevolutionary divergence between sister taxa and more distantly related species. Collectively, our results support the hypothesis that changes in horn shape-whether brought about by environmentally plastic responses, functional manipulations or evolutionary divergences-converge along 'developmental lines of least resistance', i.e. are biased by the developmental system underpinning horn shape.
... Most of the literature on phenotypic integration alone has utilized mammalian study systems such as rodents (Barrow & MacLeod, 2008;Monteiro et al., 2005), primates (Cheverud, 1982;Cheverud, 1995;Hallgrimsson et al., 2002;Mitteroecker & Bookstein, 2008;Shirai & Marroig, 2010), and carnivorans (Goswami 2006a;Goswami 2006b;Goswami & Polly, 2010a;Goswami & Polly, 2010b;Goswami et al., 2015;Randau & Goswami, 2017). Carnivora, the group that includes cats, dogs, bears, weasels, and mongooses, is a placental mammalian clade displaying great morphological and ecological variation. ...
... An extant group with a rich fossil record such as carnivorans (Goswami, 2010) indicates potential in future studies for the utilization of carnivorans as a fossil model group to apply questions of phenotypic integration. Several works on phenotypic integration have utilized extant carnivorans as a model group (Goswami, 2006a;Goswami & Polly, 2010a;Goswami & Polly, 2010b;Goswami et al., 2010;Goswami et al., 2014), fewer have applied these questions to fossil taxa (Goswami & Polly, 2010;Goswami et al., 2015). (Uyeda et al., 2017). ...
... At least for other integration metrics derived from matrix correlation analyses and pairwise trait correlations, a minimum sample size to maintain stability of these analyses is about n = 15 (Goswami, 2006a). Despite the high potential for introducing lower statistical power upon incorporating fossil taxa, fossil taxa present the only opportunity to study morphological evolution through deep time, justifying incorporation of fossil taxa into studies of morphological integration (Goswami et al., 2015). ...
Thesis
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Factors influencing greater dispersion in morphospace are a long-time interest of macroevolutionary studies, especially factors which act as constraints on adaptive exploration of morphospace. One potential factor, phenotypic integration, is often hypothesized as a constraint on the ‘evolvability’ of an organism, where less phenotypic integration results in rapid evolutionary responses to selective pressures. This hypothesis is tested by evaluating phenotypic integration and dietary ecomorphology in Mustelidae and Felidae. Felids are specialized to hypercarnivorous diets, while mustelids display a greater variety of dietary types. Therefore, mustelids are expected to display more modularity of cranial traits compared to felids which likely display higher degrees of cranial integration. A dietary ecomorphospace composed of three lower first molar diet indices was produced to calculate mean ecomorphospace distance (squared Euclidean distance) per species from the ecomorphospace centroid of each family or from a coordinate derived from ancestral state reconstruction. Using 2D geometric morphometrics of the cranial base, mean eigenvalue dispersion (SDrel(λ)) per species was calculated as an overall index of morphological integration. Ordinary least squares (OLS) and phylogenetic generalized least squares analyses (PGLS) were employed with SDrel(λ) as the explanatory variable and ecomorphospace distance as the response variable. No significant associations between cranial integration and ecomorphospace distance were detected in this work. The cranium may not be an appropriate proxy for integration, while the mammalian mandible may prove to be a more suitable component to test future hypotheses of integration. Additionally, incorporating more dietary indices based on dentition may serve to improve ecomorphological inference.
... At the evolutionary level, traits covary when they are inherited or selected jointly (Monteiro and Nogueira 2009). Taking this into account, the study of morphological integration allows shedding light on the mechanisms that work at other levels, bridging different facets of evolutionary biology (Goswami et al. 2015). Because of this, morphological integration has become a prominent concept in evolutionary biology in the last two decades (Klingenberg 2014) and many recent works have characterized large-scale patterns of integration and addressed their relationship with changes in environment (e.g., Badyaev et al. 2005), function (e.g., Young and Hallgrímsson 2005), and development (e.g., Kelly and Sears 2011;Goswami et al. 2015). ...
... Taking this into account, the study of morphological integration allows shedding light on the mechanisms that work at other levels, bridging different facets of evolutionary biology (Goswami et al. 2015). Because of this, morphological integration has become a prominent concept in evolutionary biology in the last two decades (Klingenberg 2014) and many recent works have characterized large-scale patterns of integration and addressed their relationship with changes in environment (e.g., Badyaev et al. 2005), function (e.g., Young and Hallgrímsson 2005), and development (e.g., Kelly and Sears 2011;Goswami et al. 2015). Most of these works have focused on living species, usually model organisms, but a few studies on integration in extinct taxa have been carried out in the last years (e.g., Bell et al. 2011;Maxwell and Dececchi 2013;Goswami et al. 2015), as the quantitative methods used to calculate the integration patterns can be also applied to fossils. ...
... Because of this, morphological integration has become a prominent concept in evolutionary biology in the last two decades (Klingenberg 2014) and many recent works have characterized large-scale patterns of integration and addressed their relationship with changes in environment (e.g., Badyaev et al. 2005), function (e.g., Young and Hallgrímsson 2005), and development (e.g., Kelly and Sears 2011;Goswami et al. 2015). Most of these works have focused on living species, usually model organisms, but a few studies on integration in extinct taxa have been carried out in the last years (e.g., Bell et al. 2011;Maxwell and Dececchi 2013;Goswami et al. 2015), as the quantitative methods used to calculate the integration patterns can be also applied to fossils. ...
Article
Morphological integration refers to the phenotypic interdependence of two or more traits and is estimated by the degree of covariation or correlation among traits at different levels, such as at the intraspecific and evolutionary scales. Intraspecific integration of morphological traits results from the interaction among traits at the genetic, developmental, and functional levels and it has been proposed that it channels morphological evolution by modulating variability. In this work, we test whether the intraspecific integration might have channeled the morphological evolution of the skull roof in a major tetrapod radiation, that of extinct temnospondyl amphibians. To do this, we quantified the patterns of intraspecific integration of different species and explored their relationships with the evolutionary patterns of integration and disparity of three clades of temnospondyls using geometric morphometrics. We recovered that, at the intraspecific level, the integration patterns of the total shape of the skull roof are conserved across the clade and over geological time, but that the integration among individual bones varies in every species considered. We did not find a correlation between the patterns of integration among individual bones at the intraspecific and evolutionary levels, nor between the strength of intraspecific integration of each bone and their respective disparity. These results suggest that the intraspecific integration might have not affected significantly the morphological evolution of the skull roof in temnospondyls over geological time. Thus, it seems that the morphological evolution of this skeletal part might have been driven more by selective pressures than by shared developmental constraints inherited from the temnospondyl ancestor.
... Correlated evolution among traits, known as evolutionary integration, is ubiquitous across the tree of life and can have an important impact on the trajectory of phenotypic evolution (Olson and Miller 1958;Klingenberg and Marugán-Lobón 2013;Armbruster et al. 2014;Klingenberg 2014;Goswami et al. 2014Goswami et al. , 2015Melo et al. 2016). Genetic constraints, ontogeny, and selection have pivotal roles in the development and maintenance of morphological integration over time (Arnold 1992;Arnold et al. 2001;Hansen and Houle 2004;Goswami et al. 2015;Melo et al. 2016). ...
... Correlated evolution among traits, known as evolutionary integration, is ubiquitous across the tree of life and can have an important impact on the trajectory of phenotypic evolution (Olson and Miller 1958;Klingenberg and Marugán-Lobón 2013;Armbruster et al. 2014;Klingenberg 2014;Goswami et al. 2014Goswami et al. , 2015Melo et al. 2016). Genetic constraints, ontogeny, and selection have pivotal roles in the development and maintenance of morphological integration over time (Arnold 1992;Arnold et al. 2001;Hansen and Houle 2004;Goswami et al. 2015;Melo et al. 2016). When the additive genetic covariance between traits is strong, then evolutionary correlation is likely due to genetic factors. ...
... These examples show the role of shifts in evolutionary integration associated with the evolution of novel morphologies. However, stable patterns of evolutionary integration over long time scales can be responsible for the constraint of lineages to limited regions of the morphospace and might be a plausible mechanism associated with patterns of stasis observed in the fossil record (Hansen and Houle 2004;Bolstad et al. 2014;Goswami et al. 2015). Thus, evolutionary trait correlations are central to the maintenance of form and function through time and can either drive or slow morphological differentiation. ...
Article
Correlated evolution among traits, which can happen due to genetic constraints, ontogeny, and selection, can have an important impact on the trajectory of phenotypic evolution. For example, shifts in the pattern of evolutionary integration may allow the exploration of novel regions of the morphospace by lineages. Here we use phylogenetic trees to study the pace of evolution of several traits and their pattern of evolutionary correlation across clades and over time. We use regimes mapped to the branches of the phylogeny to test for shifts in evolutionary integration while incorporating the uncertainty related to trait evolution and ancestral regimes with joint estimation of all parameters of the model using Bayesian Markov chain Monte Carlo. We implemented the use of summary statistics to test for regime shifts based on a series of attributes of the model that can be directly relevant to biological hypotheses. In addition, we extend Felsenstein's pruning algorithm to the case of multivariate Brownian motion models with multiple rate regimes. We performed extensive simulations to explore the performance of the method under a series of scenarios. Finally, we provide two test cases; the evolution of a novel buccal morphology in fishes of the family Centrarchidae and a shift in the trajectory of evolution of traits during the radiation of anole lizards to and from the Caribbean islands.
... However, while extinction is forever, it does not mean inferior. Some extinct animals could enact novel behaviors not present in modern taxa, as the fossil record is the only source of most variation in biological systems [37,21]. Biologists and bio-inspired engineers already have a firmly established and fruitful relationship. ...
... An intuitive idea in paleobiology is that organisms are made of parts, some of which are more interrelated than others. Indeed, there are methods to investigate whether and how much structures evolve together [21,40]. However, this idea is testable and quantifiable, not necessarily a clearly established rule in the body, a group of animals, or even time. ...
Article
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Animals on the visible scale have been experimenting with body form and function in enumerable enviroments for the last 540 million years. Almost all of the variation in the history of life is now gone, leaving only a tiny fraction of what is possible alive in modern animals. Recently biological and engineering techniques have made it possible to robustly answer questions only the fossil record can provide, such as the history and original functions of certain behaviors. Robotics has already begun to champion inspiration from biology, but only from the small variation seen in extant taxa. In this chapter we introduce paleontological study of a now famous source of bioinspiration: The modern African Cheetah. We discuss additional forms of high-speed pursuit predators from the lineage that demonstrate an evolutionary experiment in manuverability on uneven terrain. We also discuss how the evolution of sensing and perception does not always follow or work in concert with the evolution of the musculoskeletal system. We end by summarizing the process of our analysis so that our methods can be repeated for other animals that inspire engineers. We hope this brief primer introduces paleobiology to roboticists and demonstrates the need for biologically inspired robotics to engage with paleobiological processes, to the benefit of both robotics in developing new technology and paleobiology in answering long-standing questions about relationships between extinct forms and their functions.
... Breaking from constraints involves natural selection navigating a very specific mutational landscape, but in doing so, may improve functional efficiency, or enable a population to access unoccupied ecological niche space, ultimately fostering subsequent diversification 6 . Therefore, constraints, when broken, can lead to rapid evolutionary change in a clade and may be responsible for the unevenness in rates of taxonomic and morphological evolution observed across metazoans, providing an opportunity to explore incipient stages of diversification 7,8 . ...
... While determining the origins of integration has proved difficult (i.e., 60 ), trait integration can facilitate or limit morphological evolution depending on the direction of selection 2 . While phenotypic integration is a population-level metric, integration can have far-reaching effects on macroevolutionary processes such as taxonomic diversification, extinction, and morphological evolution 3,7 . Indeed, there is an emerging consensus that phenotypic integration can facilitate rapid and coordinated trait evolution in teleosts 5,61,62 , and may reflect a general trend across organisms 4,63,64 . ...
Article
Full-text available
Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley. Modular, rather than integrated systems are classically thought to allow functional diversity to evolve rapidly. A study of cichlid fish shows integration between divergent jaw systems at the phylogenetic, population, and genetic scales, suggesting integration can and does facilitate rapid, coordinated trait evolution.
... Thereby such responses to density may also correlate with developmental canalization and phenotypic integration. Correlations can vary with different abiotic conditions and growth stages, due to their influences on trait plasticity (Wang et al. , 2017), integration and canalization (Damiánet al. , 2018;Goswami et al ., 2015). We need more detailed studies on integration, canalization and plasticity to generalize about the relationships among them (Kavanagh, 2020), especially at different stages of plant growth or under different abiotic conditions. ...
... Correlations among trait canalization, integration and plasticity not only varied with greater densities, but such variations also change with soil conditions and growth stages. (Goswami et al. , 2015) showed an increase in correlation between fluctuating asymmetry and integration over time. But we found correlations among integration, canalization and plasticity increased over time in infertile soil, and decreased over time in fertile soil. ...
Preprint
Phenotypic integration and developmental canalization have been hypothesized to constrain the degree of phenotypic plasticity, but there is little evidence for the relationships among the three processes in different environments, especially for plants under natural conditions. To address this issue, we conducted a field experiment by subjecting plants of Abutilon theophrasti to low, medium and high densities, under infertile and fertile soil conditions, measured a variety of traits and analyzed canalization (coefficient of variation [CV]), integration (coefficient of integration [CI] and the number of significant correlations of a trait with other traits [NC]), and plasticity (REL RDPIs and ABS RDPIs) in these traits and their relationships at two stages of plant growth. Our results showed an increase in mean CV, NC and ABS RDPIs of traits with density, and the positive correlations between trait NC and ABS RDPIs became stronger with higher densities but weaker over time in fertile soil, while correlations among trait CV, NC and ABS RDPIs became stronger over time in infertile soil. Results suggested shared or cooperation mechanisms among phenotypic integration, canalization and plasticity. Soil conditions and growth stage may affect responses of these correlations to density via modifying plant size and competition strength. The attenuated canalization and enhanced integration may be helpful for the production of plasticity, especially under intense competition.
... Traditionally, morphological integration has been viewed as a set of constraints that may limit the direction and magnitude of phenotypic evolution, with the alternative to integration being body parts that evolve as separate phenotypic modules that can diverge rapidly and therefore generate disparity. [98][99][100] While the relationship between carcinization and pleonal bending appears straightforward as described above, this is not the case for the carapaces of meiurans as they exhibit substantial morphological disparity. Figures 1-3 depict rel-atively classical examples of dorsal morphology for carcinized, uncarcinized, and decarcinized taxa, but there are many exceptions within phenotypic categories (Box 1) as well as "extreme" morphologies, such as the teardrop shaped arrow crabs (the brachyuran Stenorhynchus and the squat lobster Chirostylus, not pictured) with legs more than twice the body length, or elbow crabs (Parthenopidae, not pictured) with triangular carapaces and elongated claws. ...
... However, a growing number of recent studies have uncovered strong integration of body structures alongside and even facilitating high disparity. [88,102,103] In some clades, integrated body parts may explore fewer overall directions of morphospace than independent structures, but they can attain a great range of shapes within those phenotypic constraints [99,100] (Figure 5A-C). For crabs, it has been proposed that divergent carapace shapes may help taxa invade new communities or niches where local areas of morphospace are already occupied, [104] perhaps promoting carapace disparity. ...
Article
Full-text available
A fundamental question in biology is whether phenotypes can be predicted by ecological or genomic rules. At least five cases of convergent evolution of the crab-like body plan (with a wide and flattened shape, and a bent abdomen) are known in decapod crustaceans, and have, for over 140 years, been known as "carcinization." The repeated loss of this body plan has been identified as "decarcinization." In reviewing the field, we offer phylogenetic strategies to include poorly known groups, and direct evidence from fossils, that will resolve the history of crab evolution and the degree of pheno-typic variation within crabs. Proposed ecological advantages of the crab body are summarized into a hypothesis of phenotypic integration suggesting correlated evolution of the carapace shape and abdomen. Our premise provides fertile ground for future studies of the genomic and developmental basis, and the predictability, of the crab-like body form.
... 12,13 ). Yet, the relationship between adaptive diversification and evolutionary modularity remains poorly understood 11,[14][15][16][17][18] . On the one hand, diversification into novel ecological opportunities may require changes in variational properties, in particular less constrained covariation between parts [19][20][21][22] . ...
... It is therefore plausible that the distinct evolutionary modularity of the Greater Antillean group, relative to the Primary Mainland clade, in part reflects an ancient and persistent difference in how girdles and limbs develop and grow together. Such differences in how phenotypes are generated are known to influence how evolution proceeds 13 , and will be reflected in covariation of traits across a phylogeny (i.e., evolutionary modularity and integration) 15,17,18,57 . For example, the peculiar reproductive biology of marsupials, like that of the kangaroo and its allies, is associated with weaker integration and increased modularity of fore-and hindlimbs both within and across species 58,59 (but see also ref. 60 ...
Article
Full-text available
Anolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis . This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification.
... However, modularity patterns can also shift throughout ontogeny 26 . During growth and maturation, bones arising from discrete developmental modules can group into larger, integrated (co-varied) traits 27 in response to changing selective pressures 28 . As such, modularity and integration are important drivers of phenotypic evolution, where modules with shared developmental or functional associations can be uniquely shaped by selection 25,[29][30][31] . ...
... As such, modularity and integration are important drivers of phenotypic evolution, where modules with shared developmental or functional associations can be uniquely shaped by selection 25,[29][30][31] . Evolutionary shifts in modularity have been shown to facilitate or constrain morphological variation 28,31,32 , or when selection favors similar trait integration patterns among species, can promote the evolution of convergent phenotypes 3,26,33,34 . ...
Article
Full-text available
Phenotypic convergence, describing the independent evolution of similar characteristics, offers unique insights into how natural selection influences developmental and molecular processes to generate shared adaptations. The extinct marsupial thylacine and placental gray wolf represent one of the most extraordinary cases of convergent evolution in mammals, sharing striking cranial similarities despite 160 million years of independent evolution. We digitally reconstructed their cranial ontogeny from birth to adulthood to examine how and when convergence arises through patterns of allometry, mosaicism, modularity, and integration. We find the thylacine and wolf crania develop along nearly parallel growth trajectories, despite lineage-specific constraints and heterochrony in timing of ossification. These constraints were found to enforce distinct cranial modularity and integration patterns during development, which were unable to explain their adult convergence. Instead, we identify a developmental origin for their convergent cranial morphologies through patterns of mosaic evolution, occurring within bone groups sharing conserved embryonic tissue origins. Interestingly, these patterns are accompanied by homoplasy in gene regulatory networks associated with neural crest cells, critical for skull patterning. Together, our findings establish empirical links between adaptive phenotypic and genotypic convergence and provides a digital resource for further investigations into the developmental basis of mammalian evolution.
... A preliminary study of shape evolution has been conducted on meiuran dorsal carapaces, for five brachyurans and one king crab (Scholtz et al. 2020), finding greater shape similarity between four of the brachyurans and the king crab and little between the majoid (spider or decorator crab; an example in Figure 5C) and other brachyurans. If extremes such as the spider crabs can override relationships from both phylogeny and convergence, integration of the crab body plan seems to contradict previous wisdom that described a tension between integration as a set of constraints that limit phenotypic evolution, and the alternative of separate phenotypic modules that can diverge rapidly and therefore generate disparity (Goswami et al. 2014(Goswami et al. , 2015Felice et al. 2018). However, a growing number of recent studies have uncovered strong integration of body structures alongside and even facilitating high disparity (e.g. ...
... Watanabe et al. 2019;Hedrick et al. 2020;Michaud et al. 2020). In some clades, integrated body parts may explore fewer overall directions of morphospace than independent structures, but they can attain a great range of shapes within those phenotypic constraints (Goswami et al. 2015;Felice et al. 2018; Figure 5A-C). For crabs, it has been proposed that divergent carapace shapes may help taxa invade new communities where local areas of morphospace are already occupied (Farré et al. 2020). ...
Preprint
Full-text available
A fundamental question in biology is whether phenotypes can be predicted by ecological or genomic rules. For over 140 years, convergent evolution of the crab-like body plan (with a wide and flattened shape, and a bent abdomen) at least five times in decapod crustaceans has been known as 'carcinization'. The repeated loss of this body plan has been identified as 'decarcinization'. We offer phylogenetic strategies to include poorly known groups, and direct evidence from fossils, that will resolve the pattern of crab evolution and the degree of phenotypic variation within crabs. Proposed ecological advantages of the crab body are summarized into a hypothesis of phenotypic integration suggesting correlated evolution of the carapace shape and abdomen. Our premise provides fertile ground for future studies of the genomic and developmental basis, and the predictability, of the crab-like body form.
... In contrast, when there is discordant selection on the sub-units comprising an integrated whole, the evolutionary response may be constrained. Patterns of integration and modularity are thought to evolve (Wagner and Altenberg 1996;Goswami et al. 2015). However, most studies of evolutionary modularity have focused on single clades and do not assess shifting patterns of trait correlation (although see Goswami 2006;Piras et al. 2014;Haber 2015;Anderson et al. 2016;Heck et al. 2018). ...
... intraspecific variation within a growth stage) modularity and integration as few extinct archosaurs are known from enough cranial specimens for rigorous morphometric analysis at this resolution. Furthermore, studying evolutionary integration and modularity with broad taxonomic sampling and fossil data, as in the present dataset, allows for the study of shifts in trait correlation patterns in deep time (Klingenberg 2014;Goswami et al. 2015). For each group, we established a landmarking scheme allowing for the maximum number of anatomically distinct regions to be partitioned given the presence of visible sutures in the digitized data (Electronic Supplementary Data 2). ...
Article
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 CT 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.
... Moreover, ours represents the first report of this pattern both in bats and in prenatal development. Previous studies have shown that integration canalises phenotypic variation in deep-time [59,[121][122][123][124], and that changes in size can work as evolutionary buffers for adaptive radiation [125]. Differences between morphological canalisation over deep time and our results across developmental time support the hypothesis that integration facilitates disparity from an ontogenetic perspective [59,121]. ...
... Previous studies have shown that integration canalises phenotypic variation in deep-time [59,[121][122][123][124], and that changes in size can work as evolutionary buffers for adaptive radiation [125]. Differences between morphological canalisation over deep time and our results across developmental time support the hypothesis that integration facilitates disparity from an ontogenetic perspective [59,121]. This congruence in temporal patterns differs from the mismatch in patterns of integration and disparity found across bones and modules, demonstrating that temporality rather than functionality shapes the interaction between developmental disparity and integration [49,59]. ...
Article
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Background Self-powered flight is one of the most energy-intensive types of locomotion found in vertebrates. It is also associated with a range of extreme morpho-physiological adaptations that evolved independently in three different vertebrate groups. Considering that development acts as a bridge between the genotype and phenotype on which selection acts, studying the ossification of the postcranium can potentially illuminate our understanding of bat flight evolution. However, the ontogenetic basis of vertebrate flight remains largely understudied. Advances in quantitative analysis of sequence heterochrony and morphogenetic growth have created novel approaches to study the developmental basis of diversification and the evolvability of skeletal morphogenesis. Assessing the presence of ontogenetic disparity, integration and modularity from an evolutionary approach allows assessing whether flight may have resulted in evolutionary differences in the magnitude and mode of development in bats. Results We quantitatively compared the prenatal ossification of the postcranium (24 bones) between bats (14 species), non-volant mammals (11 species) and birds (14 species), combining for the first time prenatal sequence heterochrony and developmental growth data. Sequence heterochrony was found across groups, showing that bat postcranial development shares patterns found in other flying vertebrates but also those in non-volant mammals. In bats, modularity was found as an axial-appendicular partition, resembling a mammalian pattern of developmental modularity and suggesting flight did not repattern prenatal postcranial covariance in bats. Conclusions Combining prenatal data from 14 bat species, this study represents the most comprehensive quantitative analysis of chiropteran ossification to date. Heterochrony between the wing and leg in bats could reflect functional needs of the newborn, rather than ecological aspects of the adult. Bats share similarities with birds in the development of structures involved in flight (i.e. handwing and sternum), suggesting that flight altriciality and early ossification of pedal phalanges and sternum are common across flying vertebrates. These results indicate that the developmental modularity found in bats facilitates intramodular phenotypic diversification of the skeleton. Integration and disparity increased across developmental time in bats. We also found a delay in the ossification of highly adaptable and evolvable regions (e.g. handwing and sternum) that are directly associated with flight performance. Electronic supplementary material The online version of this article (10.1186/s12862-019-1396-1) contains supplementary material, which is available to authorized users.
... Thus far, empirical studies suggest that the relationship between integration, modularity, morphological variance (disparity), and evolutionary rate varies between systems. Some studies have demonstrated an association between increased modularity and/or decreased integration with greater morphological disparity and/or rates of evolution (Claverie and Patek 2013;Goswami et al. 2015;Felice and Goswami 2018;Larouche et al. 2018). However, others have found relatively little association between integration and evolutionary trends (Goswami and Polly 2010;Sanger et al. 2012;Gerber 2013), or even positive correlations between morphological integration and disparity (Randau and Goswami 2017). ...
... As prior work shows, there is no clear rule about the impact of integration on diversification, and neither the constraint nor facilitation hypothesis have been consistently supported (Porto et al. 2008;Claverie and Patek 2013;Gerber 2013;Goswami et al. 2014Goswami et al. , 2015Evans et al. 2017). In our study, the effect of integration appears to be positive, as evidenced by the combination of higher disparity, higher net rate of evolution, and higher integration in acanthomorphs compared to nonacanthomorphs. ...
Article
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 non‐acanthomorph fishes. The main pattern of shape covariation in non‐acanthomorphs is concordant with the main trajectory of evolution between non‐acanthomorphs 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. This article is protected by copyright. All rights reserved
... Qualitative morphological analysis (Vermeij 1973), shifts in patterns displayed by discrete traits (Wagner 2018), and coordinated patterns in evolutionary disparity and rate among suites of quantitative traits (Parins-Fukuchi 2020) have all been used to reach this conclusion. Paleontological work also suggests that shifts in the strength of covariation may mediate long-term trends in phenotypic evolution (Goswami et al. 2015). A parallel but distinct avenue of research has also shown that changes in the strength of correlation between pairs of traits may underlie ecological transitions Collar 2009, Revell et al. 2022). ...
Preprint
Understanding how the intrinsic ability of populations and species to meet shifting selective demands shapes evolutionary patterns over both short and long timescales is a major question in biology. One major axis of evolutionary flexibility can be measured by phenotypic integration and modularity. The strength, scale, and structure of integration may constrain or catalyze evolution in the face of new selective pressures. We analyze a dataset of seven leaf measurements across Vitaceae to examine whether the structure of macroevolutionary integration is linked to transitions between temperate and tropical habitats by examining how the structure of integration shifts at discrete points along a phylogeny. We also examine these patterns in light of lineage diversification rates to understand how and whether patterns in the evolvability of complex multivariate phenotypes are linked to higher-level macroevolutionary dynamics. We found that shifts in the structure of macroevolutionary integration in leaves coincide with early colonization events into new climates and that lineages that are more climatically labile are more weakly integrated overall. These more evolutionarily flexible lineages also had higher lineage turnover, suggesting a link between shifting vectors of selection, internal constraint, and lineage persistence in the face of changing environments.
... That patterns of modularity are consistent in these species belonging to different orders of Trilobita raises the question of whether modularity patterns were conserved in trilobites as a whole. If this was the case, then modularity could have had significant macroevolutionary consequences over the evolutionary history of trilobites (Goswami et al., 2014(Goswami et al., , 2015. The developmental coupling of the eyes with the anteriormost region of the cranidium may have imposed a constraint on patterns of diversification that may have either impeded or enhanced the rate of evolution depending on its congruence with selective pressures (Simpson, 1944). ...
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The trilobite head served multiple functions and was composed of several fused segments. Yet, the underlying organization of the trilobite head, and whether patterns are conserved across trilobites, remains unclear. Modeling the head as being composed of modules, or subunits that vary and thus have the potential to evolve semi-independently can reveal underlying patterns of organization. Hypotheses of modular organization based on the comparative developmental biology of arthropods were evaluated using geometric morphometrics. Two-dimensional (semi)landmark datasets collected from the cranidia of two Ordovician trilobite species, Calyptaulax annulata (Phacopida) and Cloacaspis senilis (Olenida sensu Adrain, 2011) were analyzed. The degree and pattern of modularity were assessed using the covariance ratio (CR), which compares the covariation within putative modules to the covariation between them, and the fit of different models was compared using an effect size measure derived from the CR. When treating the eyes as a distinct module, the best modular hypothesis identified for C. annulata shows the eyes and anteriormost region of the head integrated as a single module. The best modular hypotheses for C. senilis are more complex but the eyes still covary mostly strongly with the anterior part of the head. The latter is also the case for all other well-supported models for both species. These results can be interpreted as a developmental signal corresponding to the anteriormost ocular segment of early arthropods that is retained throughout development, despite any likely selective pressures related to functional needs.
... If cranial asymmetries cannot be explained by injuries or disease states (see Howell, 1925), they are often proposed to offer a functional advantage (e.g., feeding efficiency; acoustic triangulation; Norberg, 1977;Benkman, 1996). In other studies, fluctuating asymmetry via intrinsic genetic factors has been identified in deep time (Goswami et al., 2015) as an explanation for developmental stability. This developmental integration, in concert with extrinsic environmental factors (Willmore et al., 2005), has also helped to explain some patterns of asymmetry observed in these groups. ...
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The cranial casques of modern cassowaries (Casuarius) have long intrigued researchers; however, in‐depth studies regarding their morphological variation are scarce. Through visual inspection, it has been recognized that casque variability exists between conspecifics. Understanding casque variation has both evolutionary and ecological importance. Although hypothesized to be targeted by selection, intraspecific casque variation has not been quantified previously. Through a large sample of C. casuarius (n = 103), we compared casque shape (lateral and rostral views) between sexes and between individuals from non‐overlapping geographical regions using two‐dimensional (2D) geometric morphometrics. We found no statistically significant differences between the casque shape of females and males and few substantial shape differences between individuals from different geographic areas. Much of the intraspecific variation within C. casuarius is due to casque asymmetries (77.5% rightward deviating, 20.7% leftward deviating, and 1.8% non‐deviating from the midline; n = 111), which explain the high variability of southern cassowary casque shape, particularly from the rostral aspect. Finally, we discuss how our non‐significant findings implicate social selection theory, and we identify the benefits of quantifying such variation for further elucidating casque function(s) and the social biology of cassowaries. Cassowary casques are among the most iconic cranial ornaments among modern Aves. Geometric morphometric shape analysis of southern cassowary ornaments indicates no sexual dimorphism and few differences between regional populations. Instead, intraspecific casque shape variation is primarily due to directional, cranial asymmetries (illustrated as five typical casque orientations referenced to a single adult skull). These data from living cassowaries are crucial to our understanding of ornament evolution and functional morphology
... Paleontologists have assessed patterns of integration and modularity within abundantly preserved species, explored differences in modularity between closely related species (Gerber and Hopkins 2011;Webster and Zelditch 2011a,b), and tracked changes in modularity and integration within lineages (Maxwell and Dececchi 2013;Goswami et al. 2015). In other cases, modularity has been assessed in extant populations and then applied to fossil taxa not normally preserved in high abundance (e.g., Young et al. 2010). ...
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The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Paleontology has a long history of investigating questions of evolvability, but paleontological thinking has tended to neglect recent discussions, because many tools used in the current evolvability literature are challenging to apply to the fossil record. The fundamental difficulty is how to disentangle whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than being due to selection and ecological success. Despite these obstacles, the fossil record offers unique and growing sources of data that capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there exist a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.
... Because these sets are primary features of the covariance structure, they should be carried on the first several principal components, and the entire eigenvalue distribution is not directly relevant. This approach to modularity has yielded powerful hypotheses of evolutionary plasticity and constraint linking development to phenotype, and to evolutionary changes in modularity over deep time (e.g., Goswami et al. 2015). Modularity models were first assessed using the RV coefficient introduced by Klingenberg (2008). ...
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This paper investigates a form of rank deficiency in phenotypic covariance matrices derived from geometric morphometric data, and its impact on measures of phenotypic integration. We first define a type of rank deficiency based on information theory, then demonstrate that this deficiency impairs the performance of phenotypic integration metrics in a model system. Lastly, we propose methods to treat for this information rank deficiency. Our first goal is to establish how the rank of a typical geometric morphometric covariance matrix relates to the information entropy of its eigenvalue spectrum. This requires clear definitions of matrix rank, of which we define three: the full matrix rank (equal to the number of input variables), the mathematical rank (the number of non-zero eigenvalues), and the information rank or ‘effective rank’ (equal to the number of non-redundant eigenvalues). We demonstrate that effective rank deficiency arises from a combination of methodological factors – Generalized Procrustes analysis, use of the correlation matrix, and insufficient sample size – as well as phenotypic covariance. Secondly, we use dire wolf jaws to document how differences in effective rank deficiency bias two metrics used to measure phenotypic integration. The eigenvalue variance characterizes the integration change incorrectly, and the standardized generalized variance lacks the sensitivity needed to detect subtle changes in integration. Both metrics are impacted by the inclusion of many small, but non-zero, eigenvalues arising from a lack of information in the covariance matrix, a problem that usually becomes more pronounced as the number of landmarks increases. We propose a new metric for phenotypic integration that combines the standardized generalized variance with information entropy. This metric is equivalent to the standardized generalized variance, but calculated only from those eigenvalues that carry non-redundant information. It is the standardized generalized variance scaled to the effective rank of the eigenvalue spectrum. We demonstrate that this metric successfully detects the shift of integration in our dire wolf sample. Our third goal is to generalize the new metric to compare data sets with different sample sizes and numbers of variables. We develop a standardization for matrix information based on data permutation, then demonstrate that Smilodon jaws are more integrated than dire wolf jaws. Finally, we describe how our information entropy-based measure allows phenotypic integration to be compared in dense semilandmark data sets without bias, allowing characterization of the information content of any given shape, a quantity we term ‘latent dispersion’.
... Paleontologists have assessed patterns of integration and modularity within abundantly preserved species, explored differences in modularity between closely related species (Gerber and Hopkins 2011;Webster and Zelditch 2011a,b), and tracked changes in modularity and integration within lineages (Maxwell and Dececchi 2013;Goswami et al. 2015). In other cases, modularity has been assessed in extant populations and then applied to fossil taxa not normally preserved in high abundance (e.g., Young et al. 2010). ...
... The rock record of the 541 million years of Earth's history throughout the Phanerozoic preserves a wide range of natural experiments (Jablonski and Shubin, 2015) affording a broad view of the environmental and evolutionary scenarios that result in different modes of evolution and their long-term outcomes. Studies of changing phenotype through geologic time have been one of the major contributions of paleontological research (Simpson, 1944;Eldredge and Gould, 1972;Williamson, 1981;Jablonski, 2005;Hopkins, 2014;Hunt and Rabosky, 2014;Goswami et al., 2015;Liow and Taylor, 2019), although much of this work has been limited to detailed analyses of a few closely related species (e.g., McNamara, 1978McNamara, , 1983Hunt et al., 2008) or broad-scale studies of bulk, generalized, or aggregate data (e. g., Foote, 1994;Korn et al., 2015). ...
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Much of the focus of palaeobiological studies in the last century can be summarized as seeking to understand how evolutionary lineages occupy new regions of morphological, ecological, and geographic space, or are excluded from those spaces. A desire to understand the processes that lead to morphological change unites a variety of biological disciplines focusing on topics ranging from studies of organism genomics to broad scale macroevolutionary analyses. There is increasing recognition that a hierarchical approach, incorporating both intrinsic genealogical processes and external ecological factors, is necessary to understand the mechanisms behind the drivers of phenotypic change. One of the most important issues that remains to be resolved regards the generation and fixation of morphological changes within evolutionary lineages, including whether the evolution of novel morphologies facilitates expansion to previously unoccupied environments (a developmental push mechanism) or whether a shift in ecological occupation results in subsequent morphologic change (an ecological pull mechanism). The geological record affords a unique perspective on morphological change, preserving both evidence of environmental change through shifts in sedimentology and the changing morphology of evolutionary lineages; as such, palaeontology provides a long-term view of the relationship between ecological and morphological shifts. This review focuses on the ways that phylogenetic palaeoecology, which utilizes phylogenetic frameworks in concert with palaeoecological data, can be leveraged to explore these questions. It begins by reviewing the literature on novelty and innovation – the origination of new morphologies and their proliferation within ecosystems – within a hierarchical framework and the role of heterochrony as the primary mechanism by which phenotypic change occurs before exploring evidence for developmental push and ecological pull as competing drivers of morphological shifts. Drivers of morphological shifts are examined through analysis of heterochronic trends in horseshoe crab evolution and comparison with case studies on angiosperm plants, giant ground sloths, and megatooth sharks.
... Nonetheless, quantifying deep-time relationships between taxonomic diversity and ecomorphology (e.g., of locomotory or feeding systems; Wainwright & Reilly, 1994) has been a primary focus of studies investigating the phenomena that promote or stabilize clade persistence (Goswami, Binder, Meachen, & O'Keefe, 2015;Higham, Birn-Jeffery, Collins, Hulsey, & Russell, 2015;Hopkins & Lidgard, 2012;Sherratt et al., 2015). For example, crocodileline archosaurs (Suchia; Figure 1) have survived numerous major extinction events, with crown crocodylians (e.g., alligators, caimans, crocodiles, and gharials) representing the result of more than 240-million years of suchian diversification . ...
Article
Effective interpretation of historical selective regimes requires comprehensive in vivo performance evaluations and well‐constrained ecomorphological proxies. The feeding apparatus is a frequent target of such evolutionary studies due to a direct relationship between feeding and survivorship, and the durability of craniodental elements in the fossil record. Among vertebrates, behaviors such as bite force have been central to evaluation of clade dynamics; yet, in the absence of detailed performance studies, such evaluations can misidentify potential selective factors and their roles. Here, we combine the results of a total‐clade performance study with fossil‐inclusive, phylogenetically informed methods to assess bite‐force proxies throughout mesoeucrocodylian evolution. Although bite‐force shifts were previously thought to respond to changing rostrodental selective regimes, we find body‐size dependent conservation of performance proxies throughout the history of the clade, indicating stabilizing selection for bite‐force potential. Such stasis reveals that mesoeucrocodylians with dietary ecologies as disparate as herbivory and hypercarnivory maintain similar bite‐force‐to‐body‐size relationships, a pattern which contrasts the precept that vertebrate bite forces should vary most strongly by diet. Furthermore, it may signal that bite‐force conservation supported mesoeucrocodylian craniodental disparity by providing a stable performance foundation for the exploration of novel ecomorphospace.
... This results in evolutionary covariances that are central to understanding phenotypic macroevolution and reflect complex interactions between genetics, morphogenesis and adaptation [1][2][3][4][5][6] . These covariances can be viewed in the context of two major concepts: integration (the extent to which traits covary) and modularity (the structure of integration within and among parts of an organism) [6][7][8][9][10][11] . Integration and modularity have frequently been studied at the within-species level, where they are thought to reflect either developmentally induced or microevolutionary covariances. ...
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Birds show tremendous ecological disparity in spite of strong biomechanical constraints imposed by flight. Modular skeletal evolution is generally accepted to have facilitated this, with distinct body regions showing semi-independent evolutionary trajectories. However, this hypothesis has received little scrutiny. We analyse evolutionary modularity and ecomorphology using three-dimensional data from across the entire skeleton in a phylogenetically broad sample of extant birds. We find strongly modular evolution of skeletal element sizes within body regions (head, trunk, forelimb and hindlimb). However, element shapes show substantially less modularity, have stronger relationships to ecology, and provide evidence that ecological adaptation involves coordinated evolution of elements across different body regions. This complicates the straightforward paradigm in which modular evolution facilitated the ecological diversification of birds. Our findings suggest the potential for undetected patterns of morphological evolution in even well-studied groups, and advance the understanding of the interface between evolutionary integration and ecomorphology.
... The avian brain, therefore, counters the notion that structures become increasingly modular through macroevolutionary time to maintain or increase evolvability (Wagner and Altenberg, 1996). Although seemingly counter-intuitive, recent empirical and simulation studies demonstrate that integrated structures have the capacity to evolve more extreme phenotypes when selection acts along major axes of variation (Villmoare, 2013;Goswami et al., 2015;Felice et al., 2018;Machado et al., 2018;Rolian, 2019). As such, the neuroanatomical diversity observed across Neornithes could still arise from strongly integrated brain structure. ...
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How do large and unique brains evolve? Historically, comparative neuroanatomical studies have attributed the evolutionary genesis of highly encephalized brains to deviations along, as well as from, conserved scaling relationships among brain regions. However, the relative contributions of these concerted (integrated) and mosaic (modular) processes as drivers of brain evolution remain unclear, especially in non-mammalian groups. While proportional brain sizes have been the predominant metric used to characterize brain morphology to date, we perform a high-density geometric morphometric analysis on the encephalized brains of crown birds (Neornithes or Aves) compared to their stem taxa—the non-avialan coelurosaurian dinosaurs and Archaeopteryx . When analyzed together with developmental neuroanatomical data of model archosaurs ( Gallus , Alligator ), crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. Furthermore, analyses by neuroanatomical regions reveal that the acquisition of this derived shape-to-size scaling relationship occurred in a mosaic pattern, where the avian-grade optic lobe and cerebellum evolved first among non-avialan dinosaurs, followed by major changes to the evolutionary and developmental dynamics of cerebrum shape after the origin of Avialae. Notably, the brain of crown birds is a more integrated structure than non-avialan archosaurs, implying that diversification of brain morphologies within Neornithes proceeded in a more coordinated manner, perhaps due to spatial constraints and abbreviated growth period. Collectively, these patterns demonstrate a plurality in evolutionary processes that generate encephalized brains in archosaurs and across vertebrates.
... Van Valkenburgh and Hertel, 1993;Binder et al., 2002;Meachen et al., 2014a;DeSantis et al., 2019), with only a few studies investigating the paleoecology of herbivores (Akersten et al., 1988;Coltrain et al., 2004;Feranec et al., 2009;Jones and DeSantis, 2017). Carnivore studies have found body size changes in Smilodon fatalis that are correlated with climate change, body size changes in Canis latrans correlated with the megafauna extinction event, and evidence that Canis dirus and Smilodon fatalis may have undergone nutrient stress, indicated by tooth breakage, tooth wear, and cortical bone thickness (Binder et al., 2002;Binder and Van Valkenburgh, 2010;Goswami et al., 2015;Meachen and Samuels, 2012;Meachen et al., 2014aMeachen et al., , 2014bO'Keefe et al., 2014;Binder et al., 2016;Van Valkenburgh and Hertel, 1993;Van Valkenburgh, 2009, but see Duckler and Van Valkenburgh, 1998;DeSantis et al., 2012DeSantis et al., , 2015 for an alternative hypothesis). While the causality of these changes in the carnivore guild at RLB has been debated, they can be informed by studies of paleoecological changes in their presumed prey. ...
Article
The Rancho La Brea locality is world famous for asphaltic deposits that trapped and preserved late Pleistocene megafauna over the last 50,000 years. This wealth of paleontological data allows for detailed investigation into paleoecological changes through the last glacial maximum into the Holocene. Here, we used dental mesowear analyses to infer dietary behavior in Bison antiquus, Equus occidentalis, and Camelops hesternus from five deposits (“pits”) spanning the latest Pleistocene: Pits 77, 91, 13, 3, and 61/67. Mesowear was compared among pits for each taxon and discriminant function and posterior probability analyses were conducted using a modern dataset to predict dietary categories at Rancho La Brea. Published mesowear scores from late Pleistocene Bison, Equus and Camelops from other localities were included in the discriminant function and posterior probability analyses to assess dietary variability among regions. Mesowear for each taxon did not differ among pits. Posterior probabilities and discriminant function analyses recovered E. occidentalis as a strict grazer with B. antiquus and C. hesternus recovered as mixed feeders. The stability of mesowear scores through the latest Pleistocene suggests average diets of these herbivores did not significantly change at Rancho La Brea. This is in contrast to documented changes in climate and flora proxies of southern California. However, it is unclear whether these proxies are representative of climate and floral changes at Rancho La Brea. Mesowear scores from late Pleistocene populations of Equus, Bison, and Camelops indicate little variability in diet in Equus, modest variability in Bison, and high variability in Camelops. These analyses suggest large ungulates may have been more opportunistic in their feeding strategies and highlights the need for using multiple proxies to clarify dietary behavior of herbivores
... More recently, the concept has also become implicit to theories of morphological integration and modularity (e.g. Goswami et al., 2015;Klingenberg, 2014). Here we explore the spatial-packing hypothesis. ...
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Networks linking single genes to multiple phenotypic outcomes can be founded on local anatomical interactions as well as on systemic factors like biochemical products. Here we explore the effects of such interactions by investigating the competing spatial demands of brain and masticatory muscle growth within the hypermuscular myostatin‐deficient mouse model and in computational simulations. Mice that lacked both copies of the myostatin gene (‐/‐) and display gross hypermuscularity, and control mice that had both copies of the myostatin gene (+/+) were sampled at 1, 7, 14 and 28 postnatal days. A total of 48 mice were imaged with standard as well as contrast‐enhanced microCT. Size metrics and landmark configurations were collected from the image data and were analysed alongside in silico models of tissue expansion. Findings revealed that: masseter muscle volume was smaller in ‐/‐ mice at day 1 but became, and remained thereafter, larger by 7 days; ‐/‐ endocranial volumes begin and remained smaller; ‐/‐ enlargement of the masticatory muscles was associated with caudolateral displacement of the calvarium, lateral displacement of the zygomatic arches, and slight dorsal deflection of the face and basicranium. Simulations revealed basicranial retroflexion (flattening) and dorsal deflection of the face associated with muscle expansion and abrogative covariations of basicranial flexion and ventral facial deflection associated with endocranial expansion. Our findings support the spatial‐packing theory and highlight the importance of understanding the harmony of competing spatial demands that can shape and maintain mammalian skull architecture during ontogeny.
... The human skull shows tremendous inter-individual variations [25,26] in its anatomy and dimensionality of the landmarks, which may be pronounced in a population representing admixture of different ethnic groups [27], as for example, Indian [28][29][30][31] and American populations [32]. Plausibly, these variations accumulated in the long course of evolution (33)(34)(35), through assimilation of co-variances [34,35] and epigenetic changes [36] in the gross and genetic structure of a population respectively, implied morphological integration [34,37]. The inclusion of variations in the skull components in the course of evolution might have subjected a population to acquire and propagate multiple errors at the molecular level [3] and to express these as aberrant genotypes and phenotypes [38], setting basis for etiogenesis of certain neuro-psychiatric disorders [7,10,12,18]. ...
Preprint
Structure - function interdependence is a universal phenomenon in biological systems. Any alteration in structural features may result in change in functions–leading to natural selection of a particular trait, or dysfunctions thereof. Many such alterations arise during the course of evolution of a species and may meticulously be traced during embryonic development of an organism. Through the theoretical construct of morphological integration, a set of phenotypic traits alter in a coordinated and integrated manner during evolution and embryonic development of an organism yielding efficient environmentally adapted physiological functions pertinent to those structures. Such integration may go awry sometimes, setting the basis for genesis of diseases. Morphological integration in human skull has been established through various methods. The brain-skull co-development is handcuffed through evolution and development, and the very basis of a neuro-psychiatric disorder could be underlying in dysmorphogenesis of the skull, its consequent effect on structures, and thus functions of the pertinent brain components. Here we propose that morphological integration in human skull may be mechanistically implied in etiogenesis of certain neuro-psychiatric disorders and should be borne in mind during clinical diagnosis and therapeutic interventions.
... Asymmetry unrelated to function is reported for other mammals (e.g. dextral twist in the rostral region of some dogs [59]) or even brought on by developmental and environmental stressors [60,61]. Further, it could be related to specific feeding strategies such as bottom-feeding or other lateralized behaviours. ...
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Background: Unlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial (nasofacial) region. This asymmetry is hypothesised to relate to echolocation, which may have evolved in the earliest diverging odontocetes. Early cetaceans (whales, dolphins, and porpoises) such as archaeocetes, namely the protocetids and basilosaurids, have asymmetric rostra, but it is unclear when nasofacial asymmetry evolved during the transition from archaeocetes to modern whales. We used three-dimensional geometric morphometrics and phylogenetic comparative methods to reconstruct the evolution of asymmetry in the skulls of 162 living and extinct cetaceans over 50 million years. Results: In archaeocetes, we found asymmetry is prevalent in the rostrum and also in the squamosal, jugal, and orbit, possibly reflecting preservational deformation. Asymmetry in odontocetes is predominant in the nasofacial region. Mysticetes (baleen whales) show symmetry similar to terrestrial artiodactyls such as bovines. The first significant shift in asymmetry occurred in the stem odontocete family Xenorophidae during the Early Oligocene. Further increases in asymmetry occur in the physeteroids in the Late Oligocene, Squalodelphinidae and Platanistidae in the Late Oligocene/Early Miocene, and in the Monodontidae in the Late Miocene/Early Pliocene. Additional episodes of rapid change in odontocete skull asymmetry were found in the Mid-Late Oligocene, a period of rapid evolution and diversification. No high-probability increases or jumps in asymmetry were found in mysticetes or archaeocetes. Unexpectedly, no increases in asymmetry were recovered within the highly asymmetric ziphiids, which may result from the extreme, asymmetric shape of premaxillary crests in these taxa not being captured by landmarks alone. Conclusions: Early ancestors of living whales had little cranial asymmetry and likely were not able to echolocate. Archaeocetes display high levels of asymmetry in the rostrum, potentially related to directional hearing, which is lost in early neocetes-the taxon including the most recent common ancestor of living cetaceans. Nasofacial asymmetry becomes a significant feature of Odontoceti skulls in the Early Oligocene, reaching its highest levels in extant taxa. Separate evolutionary regimes are reconstructed for odontocetes living in acoustically complex environments, suggesting that these niches impose strong selective pressure on echolocation ability and thus increased cranial asymmetry.
... This results in different rates and patterns of character evolution (Mitteroecker and Bookstein 2007;Klingenberg 2008), in addition to distinct patterns of homoplasy. Anatomical modules are commonly recognized in studying the evolution of form (Mitteroecker and Bookstein 2007;Cardini and Elton 2008;Klingenberg 2008;Lü et al. 2010;Goswami et al. 2011;Hopkins and Lidgard 2012;Cardini and Polly 2013;Goswami et al. 2015), and it is reasonable to suppose that such modules will contain phylogenetic characters that are more congruent with one another than with characters from other modules (Clarke and Middleton 2008). ...
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Despite the increasing importance of molecular sequence data, morphology still makes an important contribution to resolving the phylogeny of many groups, and is the only source of data for most fossils. Most systematists sample morphological characters as broadly as possible on the principle of total evidence. However, it is not uncommon for sampling to be focussed on particular aspects of anatomy, either because characters therein are believed to be more informative, or because preservation biases restrict what is available. Empirically, the optimal trees from partitions of morphological data sets often represent significantly different hypotheses of relationships. Previous work on hard-part versus soft-part characters across animal phyla revealed significant differences in about a half of sampled studies. Similarly, studies of the craniodental versus postcranial characters of vertebrates revealed significantly different trees in about one third of cases, with the highest rates observed in non-avian dinosaurs. We test whether this is a generality here with a much larger sample of 81 published data matrices across all major dinosaur groups. Using the incongruence length difference (ILD) test and two variants of the incongruence relationship difference (IRD) test, we found significant incongruence in about 50% of cases. Incongruence is not uniformly distributed across major dinosaur clades, being highest (63%) in Theropoda and lowest (25%) in Thyreophora. As in previous studies, our partition tests show some sensitivity to matrix dimensions and the amount and distribution of missing entries. Levels of homomplasy and retained synapomorphy are similar between partitions, such that incongruence must partly reflect differences in patterns of homoplasy between partitions, which may itself be a function of modularity and mosaic evolution. Finally, we implement new tests to determine which partition yields trees most similar to those from the entire matrix. Despite no bias across dinosaurs overall, there are striking differences between major groups. The craniodental characters of Ornithischia and the postcranial characters of Saurischia yield trees most similar to the 'total evidence' trees derived from the entire matrix. Trees from these same character partitions also tend to be most stratigraphically congruent: a mutual consilience suggesting that those partitions yield more accurate trees.
... Take size, for example. GM representations usually involve a size-scaling procedure, which leads many researchers to put aside isometric variation in the investigation of morphological integration, focusing on the morphological integration in shape alone (e.g., Jamniczky and Hallgrímsson 2009;Goswami et al. 2015;Curth et al. 2017;Randau et al. 2019). ILD analyses, in turn, measure traits on a ratio scale (sensu Houle et al. 2011), which leads to isometric size variation being embedded in the variation of the traits, thus leading to the joint evaluation of the overall form (size plus shape) of biological structures (e.g., Meiri et al. 2005;Young et al. 2010;Haber 2015). ...
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The magnitude of morphological integration is a major aspect of multivariate evolution, providing a simple measure of the intensity of association between morphological traits. Studies concerned with morphological integration usually translate phenotypes into morphometric representations to quantify how different morphological elements covary. Geometric and classic morphometric representations translate biological form in different ways, raising the question if magnitudes of morphological integration estimates obtained from different morphometric representations are compatible. Here we sought to answer this question by using the relative eigenvalue variance of the covariance matrix obtained for both geometric and classical representations of empirical and simulated datasets. We quantified the magnitude of morphological integration for both shape and form and compared results between representations. Furthermore, we compared integration values between shape and form to evaluate the effect of the inclusion or not of size on the quantification of the magnitude of morphological integration. Results show that the choice of morphological representation has significant impact on the integration magnitude estimate, either for shape or form. Despite this, ordination of the integration values within representations is relatively the same, allowing for similar conclusions to be reached using different methods. However, the inclusion of size in the dataset significantly changes the estimates of magnitude of morphological integration, hindering the comparison of this statistic obtained from different spaces (shape or form). Morphometricians should be aware of these differences and must consider how biological hypothesis translate into predictions about integration in each particular choice of representation. This article is protected by copyright. All rights reserved
... However, some peculiarities were observed among habitats, with higher level of FA and frequency of phenodeviants in the natural population and the most pronounced modularity/the lowest integration in urban populations. Correspondence between symmetric and asymmetric component of the shape variation is expected if development pathways are integrated, constraining evolutionary variation (Goswami et al., 2015). Our results show that patterns of the among-and within-individual variations of the common wall lizard pileus are in the concordance for all three habitat types, suggest that similar developmental mechanisms regulate head shape in different environments. ...
Article
Numerous studies of urban environment impact on wildlife imply urbanization can have both negative and positive effects. Phenotypic variation of pileus in the common wall lizard (Podarcis muralis) was analysed to determine whether urbanization levels can be associated with developmental instability induced by environmental stress. Pileus developmental pathways and instability in natural, suburban and urban populations were quantified by patterns of size and shape, fluctuating asymmetry (FA), modular organization and integration, allometric trajectories and frequency of phenodeviants. Our results show high asymmetry and modular structure of pileus with the high frequency of phenodeviants for natural, suburban and urban populations indicating elevated developmental instability in all three habitat types. However, some peculiarities were observed comparing habitats – the lowest level of FA and integration in urban populations and unexpectedly high level of FA and frequency of phenodeviants in the natural population. In addition, significant correlations between symmetric and asymmetric shape patterns, and presence of modular organization for all three habitat types suggest that genetic/environmental and developmental parcellation are somewhat aligned. Our results indicate that pileus morphology varies in a complex manner and future studies that link physiological, behavioural and morphological parameters to demographic parameters and fitness are necessary to fully understand how environmental stress affects developmental instability. Phenotypic variation of pileus in the common wall lizard (Podarcis muralis) was analyzed to determine whether urbanization levels can be associated with developmental instability induced by environmental stress. Our results show high asymmetry and modular structure of pileus with the high frequency of phenodeviants for natural, suburban and urban populations indicating elevated developmental instability in all three habitat types. However, some peculiarities were observed comparing habitats – the lowest level of FA and integration in urban populations and unexpectedly high level of FA and frequency of phenodeviants in the natural population. Our results indicate that pileus morphology varies in a complex manner and future studies that link physiological, behavioral, and morphological parameters to demographic parameters and fitness are necessary to fully understand how environmental stress affects developmental instability.
... Due to the internal architecture of developmental systems, which generates integrated modules (Goswami, Binder, Meachen, & O'Keefe, 2015;Schlichting, 1989;Wagner & Zhang, 2011), random genetic mutations may still lead to coordinated phenotypic responses (Jablonski, 2017;Moczek et al., 2011;Uller et al., 2018;West-Eberhard, 2003). For this reason, the effects of the previously cryptic genetic variation may, in fact, cause directed phenotypic change, biased towards functionally integrated phenotypes (Gerhart & Kirschner, 2007;Masel, 2006;Wagner, 2011;Watson & Szathmáry, 2016;Watson, Wagner, Pavlicev, Weinreich, & Mills, 2014). ...
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The role of developmental bias and plasticity in evolution is a central research interest in evolutionary biology. Studies of these concepts and related processes are usually conducted on extant systems and have seen limited investigation in the fossil record. Here, I identify plasticity‐led evolution (PLE) as a form of developmental bias accessible through scrutiny of paleontological material. I summarize the process of PLE and describe it in terms of the environmentally mediated accumulation and release of cryptic genetic variation. Given this structure, I then predict its manifestation in the fossil record, discuss its similarity to quantum evolution and punctuated equilibrium, and argue that these describe macroevolutionary patterns concordant with PLE. Finally, I suggest methods and directions towards providing evidence of PLE in the fossil record and conclude that such endeavors are likely to be highly rewarding. Illustration of the process of plasticity‐led evolution in terms of phenotype, environmental stress and cryptic genetic variation (CGV). Ellipses represent populations in morphospace. The shading intensity of the ellipses gives their relative level of CGV. Developmental bias may be manifest in the fossil record in patterns generated by the process of plasticity‐led evolution. Its signature is a coupling of increasing phenotypic variability and shifting phenotypic mean associated with environmental change. In a macroevolutionary context the predicted outcome of plasticity‐led evolution resembles quantum evolution and punctuated equilibrium. Developmental bias may be manifest in the fossil record in patterns generated by the process of plasticity‐led evolution. Its signature is a coupling of increasing phenotypic variability and shifting phenotypic mean associated with environmental change. In a macroevolutionary context the predicted outcome of plasticity‐led evolution resembles quantum evolution and punctuated equilibrium.
... Integration constrains the variability of individual traits, and modularity enables modules to vary and evolve independently of each other whilst still maintaining the integrity of the functional or developmental unit 4,10,11 . An integrated and modular organisation has therefore potential to affect evolutionary paths in multiple ways that include circumventing the effects of genetic pleiotropy and developmental canalisation as well as facilitating and channelling evolutionary transformations of functional and developmental units 5,12,13 . ...
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Morphological integration and modularity are important for understanding phenotypic evolution because they constrain variation subjected to selection and enable independent evolution of functional and developmental units. We report dental integration and modularity in representative otariid (Eumetopias jubatus, Callorhinus ursinus) and phocid (Phoca largha, Histriophoca fasciata) species of Pinnipedia. This is the first study of integration and modularity in a secondarily simplified dentition with simple occlusion. Integration was stronger in both otariid species than in either phocid species and related positively to dental occlusion and negatively to both modularity and tooth-size variability across all the species. The canines and third upper incisor were most strongly integrated, comprising a module that likely serves as occlusal guides for the postcanines. There was no or weak modularity among tooth classes. The reported integration is stronger than or similar to that in mammals with complex dentition and refined occlusion. We hypothesise that this strong integration is driven by dental occlusion, and that it is enabled by reduction of modularity that constrains overall integration in complex dentitions. We propose that modularity was reduced in pinnipeds during the transition to aquatic life in association with the origin of pierce-feeding and loss of mastication caused by underwater feeding.
... Although empirical analyses indicate that character-state exhaustion is the norm for fossil data [24], exhaustion/saturation does not explain the generation of new morphospace [17]. Another explanation for early bursts comes from the developmental theory used to explain decreasing rates of change [6][7][8]. Modularity treats complexes of integrated characters as semiautonomous homologies, with distinct states for individual characters appearing more often through interactions with other characters in the same module than through independent processes or interactions with characters in other modules [25]. Moreover, modules and the specific patterns of integration they entail evolve over time [5,26]. ...
Article
'Early bursts' of morphological disparity (i.e. diversity of anatomical types) are common in the fossil record. We typically model such bursts as elevated early rates of independent character change. Developmental theory predicts that modules of linked characters can change together, which would mimic the effects of elevated independent rates on disparity. However, correlated change introducing suboptimal states should encourage breakup (parcellation) of character suites allowing new (or primitive) states to evolve until new suites arise (relinkage). Thus, correlated change-breakup-relinkage presents mechanisms for early bursts followed by constrained evolution. Here, I analyse disparity in 257 published character matrices of fossil taxa. For each clade, I use inverse-modelling to infer most probably rates of independent change given both time-homogeneous and separate 'early versus late' rates. These rates are used to estimate expected disparity given both independent change models. The correlated change-breakup-relinkage model also predicts elevated frequencies of compatible character state-pairs appearing out of order in the fossil record (e.g. 01 appearing after 00 and 11; = low stratigraphic compatibility), as one solution to suboptimal states induced by correlated change is a return to states held before that change. As predicted by the correlated change-breakup-relinkage model, early disparity in the majority of clades both exceeds the expectations of either independent change model and excess early disparity correlates with low stratigraphic compatibility among character-pairs. Although it is possible that other mechanisms for linking characters contribute to these patterns, these results corroborate the idea that reorganization of developmental linkages is often associated with the origin of groups that biologists recognize as new higher taxa and that such reorganization offers a source of new disparity throughout the Phanerozoic.
... Integrative models are analyzing connections between prolonged stasis and timescale (Uyeda et al. 2011, Near et al. 2014, Pyron 2015, Price and Schmitz 2016, ecology (Stigall 2012, Price and Schmitz 2016, Lamsdell et al. 2017, and biogeography (Stigall 2012, Huang et al. 2015. Stable genetic or developmental pathways as character constellations can be analyzed in light of developmental and functional integration and modularity (Wagner 2014, Denton and Adams 2015, Rebeiz et al. 2015, Tschopp and Tabin 2017, with integration and modularity also becoming amenable to quantitative study in paleontology (Wilson 2013, Goswami et al. 2015. In summary, different disciplinary perspectives, data, and methods can be integrated within an organized structure of problems to achieve more comprehensive and unified answers to questions about slow or negligible rates of evolutionary change-stasis-for diverse kinds of parts and wholes in living systems. ...
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Biologists would be mistaken if they relegated living fossils to paleontological inquiry or assumed that the concept is dead. It is now used to describe entities ranging from viruses to higher taxa, despite recent warnings of misleading inferences. Current work on character evolution illustrates how analyzing living fossils and stasis in terms of parts (characters) and wholes (e.g., organisms and lineages) advances our understanding of prolonged stasis at many hierarchical levels. Instead of viewing the concept's task as categorizing living fossils, we show how its primary role is to mark out what is in need of explanation, accounting for the persistence of both molecular and morphological traits. Rethinking different conceptions of living fossils as specific hypotheses reveals novel avenues for research that integrate phylogenetics, ecological and evolutionary modeling, and evo-devo to produce a more unified theoretical outlook.
... More specifically, it is suggested that the fragmentation of trait relationships into semi-autonomous units, or modules, promotes evolvability by releasing sets of traits with divergent selection pressures from the constraints of their covariation, imposed by genetic pleiotropy or developmental canalization (Wagner and Altenberg 1996). Assessing the accuracy of this hypothesis and understanding how prevalent these various potential effects of trait integration are in the natural world requires comparative data across taxa to reconstruct the patterns of trait relationships, how they change, and how they relate to macroevolutionary patterns in organismal form and disparity (Conner et al. 2014;Goswami et al. 2015). While a rich literature exists for examining genetic and developmental associations and their relationship to phenotypic integration at a microevolutionary scale, there is yet relatively little broad comparative data for phenotypic integration and even less incorporation of this field within the study of morphological evolution at the macroevolutionary scale. ...
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Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium. This article is protected by copyright. All rights reserved
... In the absence of models that can predict patterns of variability, empiricists are often limited to comparing phenotypes within populations or species with the pattern of phenotypic diversification across species (Klingenberg 2014;Goswami et al. 2015). Although this risks confounding variation and variability (Box 1), phenotypic covariance in morphological characters in extant vertebrates has been demonstrated to be concordant with the patterns of historical diversification, including for example pharyngeal jaw morphology in cichlids (Muschick et al. 2011), beak shape in raptors (Bright et al. 2016), skull morphology in toads (Simon et al. 2016), and body shape in sticklebacks (Schluter 1996). ...
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A recurrent theme in evolutionary biology is to contrast natural selection and developmental constraint – two forces pitted against each other as competing explanations for organismal form. Despite its popularity, this juxtaposition is deeply misleading.... Phenotypic variation is generated by the processes of development, with some variants arising more readily than others—a phenomenon known as “developmental bias.” Developmental bias and natural selection have often been portrayed as alternative explanations, but this is a false dichotomy: developmental bias can evolve through natural selection, and bias and selection jointly influence phenotypic evolution. Here, we briefly review the evidence for developmental bias and illustrate how it is studied empirically. We describe recent theory on regulatory networks that explains why the influence of genetic and environmental perturbation on phenotypes is typically not uniform, and may even be biased toward adaptive phenotypic variation. We show how bias produced by developmental processes constitutes an evolving property able to impose direction on adaptive evolution and influence patterns of taxonomic and phenotypic diversity. Taking these considerations together, we argue that it is not sufficient to accommodate developmental bias into evolutionary theory merely as a constraint on evolutionary adaptation. The influence of natural selection in shaping developmental bias, and conversely, the influence of developmental bias in shaping subsequent opportunities for adaptation, requires mechanistic models of development to be expanded and incorporated into evolutionary theory. A regulatory network perspective on phenotypic evolution thus helps to integrate the generation of phenotypic variation with natural selection, leaving evolutionary biology better placed to explain how organisms adapt and diversify.
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Analysis of trait covariation plays a pivotal role in the study of phenotypic evolution. The magnitude of covariation is often quantified with statistics based on dispersion of eigenvalues of a covariance or correlation matrix—eigenvalue dispersion indices. This study clarifies the statistical justifications of these statistics and elaborates on their sampling properties. The relative eigenvalue variance of a covariance matrix is known in the statistical literature a test statistic for sphericity, thus is an appropriate measure of eccentricity of variation. The same of a correlation matrix is equal to the average squared correlation, which has a straightforward interpretation as a measure of integration. Here, expressions for the mean and variance of these statistics are analytically derived under multivariate normality, clarifying the effects of sample size N, number of variables p, and parameters on sampling bias and error. Simulations confirm that approximations involved are reasonably accurate with a moderate sample size (N ≥ 16–64). Importantly, sampling properties of these indices are not adversely affected by a high p:N ratio, promising their utility in high-dimensional phenotypic analyses. They can furthermore be applied to shape variables and phylogenetically structured data with appropriate modifications.
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Developmental modularity, i.e., coherent organization and function of developmentally related traits, is an emergent property of organismic development and evolution. However, knowledge about how modular variation and evolution are driven genetically is still limited. Here, using ornamental plants as an example, we propose a computational framework to map, visualize and annotate the genetic architecture of trait modularity by integrating modularity theory into system mapping, a statistical model for multifaceted genetic mapping of complex traits. A developmental module can be viewed as an ecosystem, in which the constituting components compete for space and resources or cooperate symbiotically to organize its function and behavior. This interactive process is quantified by mathematical models and evolutionarily interpreted by game theory. The proposed framework can test whether and how genes regulate the coordination of different but interconnected traits through their competition or cooperation to downstream developmental modularity.
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How do large and unique brains evolve? Historically, comparative neuroanatomical studies have attributed the evolutionary genesis of highly encephalized brains to deviations along, as well as from, conserved scaling relationships among brain regions. However, the relative contributions of these concerted (integrated) and mosaic (modular) processes as drivers of brain evolution remain unclear, especially in non-mammalian groups. While proportional brain sizes have been the predominant metric used to characterize brain morphology to date, we perform a high-density geometric morphometric analysis on the encephalized brains of crown birds (Neornithes or Aves) compared to their stem taxa—the non-avialan coelurosaurian dinosaurs. When analyzed together with developmental neuroanatomical data of model archosaurs ( Gallus , Alligator ), crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. Furthermore, analyses by neuroanatomical regions reveal that the acquisition of this derived shape-to-size scaling relationship occurred in a mosaic pattern, where the ‘avian’-grade optic lobe and cerebellum evolved first among non-avialan dinosaurs, followed by major changes to the evolutionary and developmental dynamics of cerebrum shape after the origin of Avialae. Notably, the brain of crown birds is a more integrated structure than non-avialan archosaurs, implying that diversification of brain morphologies within Neornithes proceeded in a more coordinated manner, perhaps due to spatial constraints and abbreviated growth period. Collectively, these patterns demonstrate a plurality in evolutionary processes that generate encephalized brains in archosaurs and across vertebrates.
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The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Although paleontology has a long history of investigating questions of evolvability, often invoking different but allied terminology, the study of evolvability in the fossil record has seemed intrinsically problematic. How can we surmount difficulties in disentangling whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than due to selection and ecological success? Despite these challenges, the fossil record is unique in offering growing sources of data that span millions of years and therefore capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there are a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.
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The skeleton is a complex arrangement of anatomical structures that covary to various degrees depending on both intrinsic and extrinsic factors. Among the Feliformia, many species are characterized by predator lifestyles providing a unique opportunity to investigate the impact of highly specialized hypercarnivorous diet on phenotypic integration and shape diversity. To do so, we compared the shape of the skull, mandible, humerus, and femur of species in relation to their feeding strategies (hypercarnivorous vs. generalist species) and prey preference (predators of small vs. large prey) using three-dimensional geometric morphometric techniques. Our results highlight different degrees of morphological integration in the Feliformia depending on the functional implication of the anatomical structure, with an overall higher covariation of structures in hypercarnivorous species. The skull and the forelimb are not integrated in generalist species, whereas they are integrated in hypercarnivores. These results can potentially be explained by the different feeding strategies of these species. Contrary to our expectations, hypercarnivores display a higher disparity for the skull than generalist species. This is probably due to the fact that a specialization toward high-meat diet could be achieved through various phenotypes. Finally, humeri and femora display shape variations depending on relative prey size preference. Large species feeding on large prey tend to have robust long bones due to higher biomechanical constraints.
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Pleistocene glacial cycles are thought to have driven ecological niche shifts, including novel niche formation. North American pine martens, Martes americana and M. caurina, are exemplar taxa thought to have diverged molecularly and morphologically during Pleistocene glaciation. Previous research found correlations between Martes limb morphology with biome and climate, suggesting that appendicular evolution may have occurred via adaptation to selective pressures imposed by novel and shifting habitats. Such variation can also be achieved through non-adaptive means such as genetic drift. Here, we evaluate whether regional genetic differences reflect limb morphology differences among populations of M. americana and M. caurina by analyzing evolutionary tempo and mode of six limb elements. Our comparative phylogenetic models indicate that genetic structure predicts limb shape better than size. Marten limb size has low phylogenetic signal, and the best supported model of evolution is punctuational (kappa), with morphological and genetic divergence occurring simultaneously. Disparity through time analysis suggests that the tempo of limb evolution in Martes tracks Pleistocene glacial cycles, such that limb size may be responding to shifting climates rather than population genetic structure. Contrarily, we find that limb shape is strongly tied to genetic relationships, with high phylogenetic signal and a lambda mode of evolution. Overall, this pattern of limb size and shape variation may be the result of geographic isolation during Pleistocene glacial advance, while declines in disparity suggest hybridization during interglacial periods. Future inclusion of extinct populations of Martes, which were more morphologically and ecologically diverse, may further clarify Martes phenotypic evolution.
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Differences among clades in their diversification patterns result from a combination of extrinsic and intrinsic factors. In this study I examined the role of intrinsic factors in the morphological diversification of ruminants in general, and in the differences between bovids and cervids in particular. Using skull morphology, which embodies many of the adaptations that distinguish bovids and cervids, I examined 132 of the 200 extant ruminant species. As a proxy for intrinsic constraints I quantified different aspects of the phenotypic covariation structure within species, and compared them with the among-species divergence patterns, using phylogenetic comparative methods. My results show that for most species, divergence is well aligned with their phenotypic covariance matrix, and those that are better aligned have diverged further away from their ancestor. Bovids have dispersed into a wider range of directions in morphospace than cervids, and their overall disparity is higher. This difference is best explained by the lower eccentricity of bovids within-species covariance matrices. These results are consistent with the role of intrinsic constraints in determining amount, range, and direction of dispersion, and demonstrate that intrinsic constraints can influence macroevolutionary patterns even as the covariance structure evolves.
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A major goal in post‐synthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: 1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; 2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a ‘preadaptive’ effect by catalyzing later episodes of dramatic morphological remodeling. This article is protected by copyright. All rights reserved
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A fuller understanding of the role of developmental bias in shaping large‐scale evolutionary patterns requires integrating bias (the probability distribution of variation accessible to an ancestral phenotype) with clade dynamics (the differential survival and production of species and evolutionary lineages). This synthesis could proceed as a two‐way exchange between the developmental data available to neontologists and the strictly phenotypic but richly historical and dynamic data available to paleontologists. Analyses starting in extant populations could aim to predict macroevolution in the fossil record from observed developmental bias, while analyses starting in the fossil record, particularly the record of extant species and lineages, could aim to predict developmental bias from macroevolutionary patterns, including the broad range of extinct phenotypes. Analyses in multivariate morphospaces are especially effective when coupled with phylogeny, theoretical and developmental models, and diversity–disparity plots. This research program will also require assessing the “heritability” of an ancestral bias across phylogeny, and the tendency for bias change in strength and orientation over evolutionary time. Such analyses will help find a set of general rules for the macroevolutionary effects of developmental bias, including its impact on and interactions with the other intrinsic and extrinsic factors governing the movement, expansion, and contraction of clades in morphospace. HIGHLIGHTS • A fuller, more synthetic understanding of the macroevolutionary role of developmental bias requires the integration of bias with clade dynamics—that is, the differential survival and production of species and evolutionary lineages
Chapter
Functional loading generates stress and strain within the skeleton. Deducing how the skull stresses and strains has the potential to inform on what feeding and other behavioural loads the skeleton can withstand and the functional consequences of changes to shape. When applied in deep time, mechanical analysis of the skeleton may be used to determine the function of extinct organisms but also higher level questions such as niche partitioning, the evolutionary relationship between form, function and disparity, rates of functional evolution and the influence of constraints on morphological evolution. One method for deducing stress and strain in complex structures is finite element (FE) analysis. FE models have the potential to address questions of the evolution of form and function in vertebrates, but it is important to consider the assumptions and potential errors involved in creating and analysing FE simulations of function and behaviour. Currently lacking is an understanding of phylogenetic variability in various FE model input parameters such as bone material properties, muscle stress and adductor muscle pennation and fibre lengths. How within-species mechanical function relates to across-species function is still largely unknown. However, if the accuracy of an FE model can be estimated, then it is possible to frame appropriate questions to test long-standing functional hypotheses and deduce pattern and process in the relationship between form and function.
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There is abundant theoretical and empirical evidence for the influence of variational properties of populations on microevolution, and more limited support for their lasting impact during macroevolution. This study applies evolutionary quantitative genetic approaches to assess the long‐term impact of within‐population phenotypic variation and covariation (the P matrix) on population divergence in recent humans and species diversification in genus Homo. Similarity between the primary axes of within‐ and between‐population craniofacial variation confirms a role for pmax in human population divergence, although diversification is not constrained to be unidimensional. The long term impact of the P matrix on craniofacial evolution is supported by higher‐than‐average evolvabilities along most branches of the Homo tree, but statistical uncertainty inherent in the data reduce confidence in this conclusion. Higher evolvability is not statistically correlated with increased rate of evolution, although the relationship is in the predicted direction. This is due in part to the high evolutionary rate on the early modern human branch despite its moderate level of evolvability. There was evidence for neutral evolution as well as directional and stabilizing selection over the Plio‐Pleistocene using generalized genetic distance as a test statistic. This article is protected by copyright. All rights reserved
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The evolutionary diversification of birds has been facilitated by specializations for various locomotor modes, with which the proportion of the limb skeleton is closely associated. However, recent studies have identified phylogenetic signals in this system, suggesting the presence of historical factors that have affected its evolutionary variability. In this study, in order to explore potential roles of ontogenetic integration in biasing the evolution in the avian limb skeleton, evolutionary diversification patterns in six avian families (Anatidae, Procellariidae, Ardeidae, Phalacrocoracidae, Laridae, and Alcidae) were examined and compared to the postnatal ontogenetic trajectories in those taxa, based on measurement of 2641 specimens and recently collected ontogenetic series, supplemented by published data. Morphometric analyses of lengths of six limb bones (humerus, ulna, carpometacarpus, femur, tibiotarsus, and tarsometatarsus) demonstrated that: 1) ontogenetic trajectories are diverse among families; 2) evolutionary diversification is significantly anisotropic; and, most importantly, 3) major axes of evolutionary diversification are correlated with clade‐specific ontogenetic major axes in the shape space. These results imply that the evolutionary variability of the avian limbs has been biased along the clade‐specific ontogenetic trajectories. It may explain peculiar diversification patterns characteristic to some avian groups, including the long‐leggedness in Ardeidae and tendency for flightlessness in Anatidae.
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Background: Although variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.Principal Findings: We used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.Conclusions: This analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.
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Although most studies on integration and modularity have focused on variation among individuals within populations or species, this is not the only level of variation for which integration and modularity exist. Multiple levels of biological variation originate from distinct sources: genetic variation, phenotypic plasticity resulting from environmental heterogeneity, fluctuating asymmetry from random developmental variation and, at the interpopulation or interspecific levels, evolutionary change. The processes that produce variation at all these levels can impart integration or modularity on the covariance structure among morphological traits. In turn, studies of the patterns of integration and modularity can inform about the underlying processes. In particular, the methods of geometric morphometrics offer many advantages for such studies because they can characterize the patterns of morphological variation in great detail and maintain the anatomical context of the structures under study. This paper reviews biological concepts and analytical methods for characterizing patterns of variation and for comparing across levels. Because research comparing patterns across level has only just begun, there are relatively few results, generalizations are difficult and many biological and statistical questions remain unanswered. Nevertheless, it is clear that research using this approach can take advantage of an abundance of new possibilities that are so far largely unexplored.
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Despite the long-standing interest of biologists in patterns of correlation and phenotypic integration, little attention has been paid to patterns of correlation across a broad phylogenetic spectrum. We report analyses of mean phenotypic correlations among a variety of linear measurements from a wide diversity of plants and animals, addressing questions about function, development, integration and modularity. These analyses suggest that vertebrates, hemimetabolous insects and vegetative traits in plants have similar mean correlations, around 0.5. Traits of holometabolous insects are much more highly correlated, with a mean correlation of 0.84; this may be due to developmental homeostasis caused by lower spatial and temporal environmental variance during complete metamorphosis. The lowest mean correlations were those between floral and vegetative traits, consistent with Berg's ideas about functional independence between these modules. Within trait groups, the lowest mean correlations were among vertebrate head traits and floral traits (0.38-0.39). The former may be due to independence between skull modules. While there is little evidence for floral integration overall, certain sets of functionally related floral traits are highly integrated. A case study of the latter is described from wild radish flowers.
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Integration and modularity refer to the patterns and processes of trait interaction and independence. Both terms have complex histories with respect to both conceptualization and quantification, resulting in a plethora of integration indices in use. We review briefly the divergent definitions, uses and measures of integration and modularity and make conceptual links to allometry. We also discuss how integration and modularity might evolve. Although integration is generally thought to be generated and maintained by correlational selection, theoretical considerations suggest the relationship is not straightforward. We caution here against uncontrolled comparisons of indices across studies. In the absence of controls for trait number, dimensionality, homology, development and function, it is difficult, or even impossible, to compare integration indices across organisms or traits. We suggest that care be invested in relating measurement to underlying theory or hypotheses, and that summative, theory-free descriptors of integration generally be avoided. The papers that follow in this Theme Issue illustrate the diversity of approaches to studying integration and modularity, highlighting strengths and pitfalls that await researchers investigating integration in plants and animals.
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Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.
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The tar pits of Rancho La Brea are a unique window onto the biology and ecology of the terminal Pleistocene in southern California. In this study we capitalize on recent advances in understanding of La Brea tar pit chronology to perform the first morphometric study of crania of the dire wolf, Canis dirus, over time. We first present new data on tooth fracture and wear from pits dated older than heretofore analyzed, and demonstrate that fracture and wear events, and the increased competition and heightened carcass utilization they are thought to represent, were of varying intensity across the sampled time intervals. Skull size, and by extension body size, is shown to differ significantly among pits at La Brea, with the strongest single observation being reduction in body size at the last glacial maximum. Skull size variation is shown to be a result of both ontogenetic and evolutionary factors, neither of which is congruent with a temporal version of Bergmann's rule. Skull shape difference among the pits is also significant, with shape variability attributable to both neotenic effects in populations with high breakage and wear, and evolutionary changes possibly due to climate change. Testing of this hypothesis requires better accuracy and precision in La Brea carbon data, a program that is within the reach of current AMS dating technology.
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Morphological integration and modularity are closely related concepts about how different traits of an organism are correlated. Integration is the overall pattern of intercorrelation; modularity is the partitioning of integration into evolutionarily or developmentally independent blocks of traits. Modularity and integration are usually studied using quantitative phenotypic data, which can be obtained either from extant or fossil organisms. Many methods are now available to study integration and modularity, all of which involve the analysis of patterns found in trait correlation or covariance matrices. We review matrix correlation, random skewers, fluctuating asymmetry, cluster analysis, Euclidean distance matrix analysis (EDMA), graphical modelling, two-block partial least squares, RV coefficients, and theoretical matrix modelling and discuss their similarities and differences. We also review different coefficients that are used to measure correlations. We apply all the methods to cranial landmark data from and ontogenetic series of Japanese macaques, Macaca fuscata to illustrate the methods and their individual strengths and weaknesses. We conclude that the exploratory approaches (cluster analyses of various sorts) were less informative and less consistent with one another than were the results of model testing or comparative approaches. Nevertheless, we found that competing models of modularity and integration are often similar enough that they are not statistically distinguishable; we expect, therefore, that several models will often be significantly correlated with observed data.
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The concept of morphological integration describes the pattern and the amount of correlation between morphological traits. Integration is relevant in evolutionary biology as it imposes constraint on the variation that is exposed to selection, and is at the same time often based on heritable genetic correlations. Several measures have been proposed to assess the amount of integration, many using the distribution of eigenvalues of the correlation matrix. In this paper, we analyze the properties of eigenvalue variance as a much applied measure. We show that eigenvalue variance scales linearly with the square of the mean correlation and propose the standard deviation of the eigenvalues as a suitable alternative that scales linearly with the correlation. We furthermore develop a relative measure that is independent of the number of traits and can thus be readily compared across datasets. We apply this measure to examples of phenotypic correlation matrices and compare our measure to several other methods. The relative standard deviation of the eigenvalues gives similar results as the mean absolute correlation (W.P. Cane, Evol Int J Org Evol 47:844–854, 1993) but is only identical to this measure if the correlation matrix is homogenous. For heterogeneous correlation matrices the mean absolute correlation is consistently smaller than the relative standard deviation of eigenvalues and may thus underestimate integration. Unequal allocation of variance due to variation among correlation coefficients is captured by the relative standard deviation of eigenvalues. We thus suggest that this measure is a better reflection of the overall morphological integration than the average correlation.
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Phenotypic integration can influence evolutionary rate and direction by channeling variation into few dimensions. The extent to which that channeling serves as a constraint over macroevolutionary timescales is determined in part by the evolutionary lability of phenotypic integration. Evolutionary change in patterns of pleiotropy, potentially reducing that constraint, is thought to be more readily achieved when pleiotropy is structured by variation arising in parallel along different developmental pathways rather than by variation arising from direct interactions within and between those pathways. Herein we test two predictions that follow from that hypothesis: (1) that clades undergoing dramatic diversification are characterized by integration that is weakly influenced by direct interactions; and (2) that the structure of integration arising from direct interactions is more conservative than that arising from parallel variation. We examine integration of the cranidium of two Cambrian ptychoparioid trilobites, Crassifimbra walcotti and Eokochaspis nodosa, comparing them to each other and to a previously studied species, C.? metalaspis. Shape variation is decomposed into components representing variation among individuals and variation due to direct interactions. In all three species, variation among individuals was only weakly influenced by direct interactions, suggesting that integration was unlikely to have been a long-term constraint on the Cambrian diversification of ptychoparioids. Phenotypic integration of E. nodosa is no more similar than expected by chance to either Crassifimbra species, but the component due to direct interactions is more similar than expected by chance to that of C.? metalaspis. Conversely, the two Crassifimbra species are generally similar (although not identical) in phenotypic integration, but markedly differ in their structure of direct interactions. Integration arising from direct interactions was therefore not immune to restructuring over even short evolutionary timescales, and was not always more conservative than that arising from parallel variation. KeywordsIntegration–Modularity–Cambrian–Trilobites–Evolution–Morphometrics
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Shape variation in the vertebrate skull is often studied by considering this bony structure as a single discrete unit, but it can also be interpreted exploring covariation among functionally and developmentally distinct regions, or modules. In this paper, we explore the evolution of skull shape in extant and fossil carnivoran cats by looking at covariation between two distinct modules: the rostrum (splanchnocranium) and braincase (neurocranium). Previous work suggests that the evolution of extreme skull shapes in sabertoothed cats may occur along developmental axes similar to the allometric trajectory observed for extant conical-toothed cats. Here, we reassess this hypothesis by using geometric morphometric data to test for covariation between rostral and braincasemodules in sabertoothed and conical-toothed cats. Using partial least squares analysis, we detect a correlated pattern of evolution between rostrum and braincase shape in both forms. However, when we compare within module integration between conical and sabertoothed cats, we find significant differences in vector trajectories for the rostrum but not the braincase. Both skull modules of conical-toothed cats are more influenced by allometry. For sabertoothed taxa, relative canine height drives shape in the rostrum, but both size and canine length affect braincase shape. We suggest that sabertoothed skull morphology is the result of genetic and developmental processes that were affected by the growth rate of the upper canines. The striking convergence between independent sabertooth radiations indicates that elongation of the canines influenced interspecific skull shape variation in different lineages but in a similar way.
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Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development. An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification). The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.
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Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.
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Are measurements of quantitative genetic variation useful for predicting long-term adaptive evolution? To answer this question, I focus on gmax , the multivariate direction of greatest additive genetic variance within populations. Original data on threespine sticklebacks, together with published genetic measurements from other vertebrates, show that morphological differentiation between species has been biased in the direction of gmax for at least four million years, despite evidence that natural selection is the cause of differentiation. This bias toward the direction of evolution tends to decay with time. Rate of morphological divergence between species is inversely proportional to θ, the angle between the direction of divergence and the direction of greatest genetic variation. The direction of greatest phenotypic variance is not identical with gmax , but for these data is nearly as successful at predicting the direction of species divergence. I interpret the findings to mean that genetic variances and covariances constrain adaptive change in quantitative traits for reasonably long spans of time. An alternative hypothesis, however, cannot be ruled out: that morphological differentiation is biased in the direction gmax because divergence and gmax are both shaped by the same natural selection pressures. Either way, the results reveal that adaptive differentiation occurs principally along "genetic lines of least resistance."
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Morphological integration and modularity have become central concepts in evolutionary biology and geometric morphometrics. This review summarizes the most frequently used methods for characterizing and quantifying integration and modularity in morphometric data: principal component analysis and related issues such as the variance of eigenvalues, partial least squares, comparison of covariation among alternative partitions of landmarks, matrix correlation and ordinations of covariance matrices. Allometry is often acting as an integrating factor. Integration and modularity can be studied at different levels: developmental integration is accessible through analyses of covariation of fluctuating asymmetry, genetic integration can be investigated in different experimental protocols that either focus on effects of individual genes or consider the aggregate effect of the whole genome, and several phylogenetic comparative methods are available for studying evolutionary integration. Morphological integration and modularity have been investigated in many species of mammals The review gives a survey of geometric morphometric studies in some of the groups for which many studies have been published: mice and other rodents, carnivorans, shrews, humans and other primates. This review demonstrates that geometric morphometrics offers an established methodology for studying a wide range of questions concerning integration and modularity, but also points out opportunities for further innovation.
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Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional an