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Abstract

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.
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... Several morphological traits in non-avialan dinosaurs are known to be paedomorphic or peramorphic. [50][51][52][53] However, the functional significance of these traits has not been quantified, and thus their evolutionary trends remain unclear, given bone morphology and function may not be tightly linked. 54 This study represents an initial attempt to quantify a heterochronic pattern from a functional perspective, which demonstrates how ''functional peramorphosis'' could have facilitated the mandibular evolution of non-avialan theropods. ...
... 1,2 The tyrannosauroids Tyrannosaurus rex and Tarbosaurus bataar were chosen for ontogenetic comparison as only these theropod species preserve complete mandibles with age estimations based on histological analysis. 44,50,51 The five clades are classified into two dietary groups-carnivory (Tyrannosauroidea, Dromaeosauridae) and herbivory (Ornithomimosauria, Therizinosauria, Oviraptorosauria)-based on previous inferences encompassing extrinsic, anatomical, statistical and biomechanical evidence. 5 ...
Article
Theropod dinosaurs underwent some of the most remarkable dietary changes in vertebrate evolutionary history, shifting from ancestral carnivory1, 2, 3 to hypercarnivory⁴,⁵ and omnivory/herbivory,6, 7, 8, 9 with some taxa eventually reverting to carnivory.10, 11, 12 The mandible is an important tool for food acquisition in vertebrates and reflects adaptations to feeding modes and diets.¹³,¹⁴ The morphofunctional modifications accompanying the dietary changes in theropod dinosaurs are not well understood because most of the previous studies focused solely on the cranium and/or were phylogenetically limited in scope,¹²,15, 16, 17, 18, 19, 20, 21 while studies that include multiple clades are usually based on linear measurements and/or discrete osteological characters.⁸,²² Given the potential relationship between macroevolutionary change and ontogenetic pattern,²³ we explore whether functional morphological patterns observed in theropod mandibular evolution show similarities to the ontogenetic trajectory. Here, we use finite element analysis to study the mandibles of non-avialan coelurosaurian theropods and demonstrate how feeding mechanics vary between dietary groups and major clades. We reveal an overall reduction in feeding-induced stresses along all theropod lineages through time. This is facilitated by a post-dentary expansion and the development of a downturned dentary in herbivores and an upturned dentary in carnivores likely via the “curved bone effect.” We also observed the same reduction in feeding-induced stress in an ontogenetic series of jaws of the tyrannosaurids Tarbosaurus and Tyrannosaurus, which is best attributed to bone functional adaptation. This suggests that this common tendency for structural strengthening of the theropod mandible through time, irrespective of diet, is linked to “functional peramorphosis” of bone functional adaptations acquired during ontogeny.
... This claimed was mostly based on observations that the adult SB-charr morphology corresponded to embryonic or juvenile characters in salmonids, suggesting that the retention of early traits (i.e., paedomorphosis) may be involved in the phenotypic differentiation of the charr morphs . Paedomorphosis is a remarkable example of the interactions between developmental and evolutionary processes, which have been proposed as a catalyst of adaptive divergence in other taxa (Bhullar et al., 2012), making heterochrony in development a very tempting hypothesis to explain the developmental origin phenotypic diversity in the Arctic charr of Thingvallavatn. However, more recent commongarden experiments showed on that embryos of all four morphs have rather similar ontogenetic trajectories of their craniofacial morphology, although LB-embryos significantly differed from PL-and SB-charr in several aspects of such trajectories Ponsioen, 2020). ...
... Extensive research efforts have been dedicated over the past few years to understand the evolution of ontogenetic differences between populations, mainly with the aim to unravel the processes of adaptive divergence and speciation (Abzhanov, Protas, Grant, Grant, & Tabin, 2004;Adams & Nistri, 2010;Beck et al., 2019;Bhullar et al., 2012;Cooper et al., 2010;Currey, Bassham, Perry, & Cresko, 2017;Parsons et al., 2014;Roberts, Hu, Albertson, & Kocher, 2011;Santos-Santos, Audenaert, Verheyen, & Adriaens, 2021;. However, significant knowledge gaps remain on the importance of development in adaptive divergence, notably on the role of canalization, that is, the buffering phenotypic variability in response to genetic and environmental variations (Hallgrímsson et al., 2002;Pesevski & Dworkin, 2020;Waddington, 1942). ...
Thesis
The theory of divergence by trophic polymorphism, an important part of diversification in vertebrates, has recently been extended to encompass the interplay of developmental, ecological and evolutionary processes (Eco-Evo-Devo dynamics). However, this extended theory doesn’t thoroughly explain the evolution of reproductive isolation, which is unfortunate considering the recent advances from the field of speciation. In this thesis, I argue that the Arctic charr morphs of Thingvallavatn are an ideal system to study how reproductive isolation is embedded within the theory of divergence by resource polymorphism, which I present through five papers. First, I focused on two sympatric morphs, the small-benthic (SB) and the planktivorous (PL) charr. Common-garden experiments showed limited evidence for hybridization to affect the structure of trait covariance in both morphs, regarding morphology, developmental timing and feeding behaviour (Paper I), and personality traits (Paper II). However, information on gene expression variability in embryos indicated that hybridization might influence evolvability (Paper III). Multiple reproductive barriers between the two morphs, involving habitat use, assortative mating and hybrid development were also assessed (Paper IV). Finally, Paper V combines field studies and rearing experiments to explore the interplay between habitat choice and offspring development in the large-benthic (LB) charr, which spawns earlier in the season than the other morphs. The results suggested that LB-charr favour temperature conditions that may delay offspring development. Altogether, these findings provide an overview on reproductive isolation among the Arctic charr morphs of Thingvallavatn and constitute a primer to study speciation in an Eco-Evo-Devo context.
... Because different environments and behaviours place different demands on the functional mechanics and physiologies of organisms, it is expected that body proportions should vary across animals occupying different ecological niches [8][9][10][11][12][13][14] . However, modification of body size and shape by ecological pressures may also be constrained by other factors, notably phylogenetic history and the ecological trajectory of evolutionary change 3,15,16 . ...
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Body size and shape play fundamental roles in organismal function and it is expected that animals may possess body proportions that are well-suited to their ecological niche. Tetrapods exhibit a diverse array of body shapes, but to date this diversity in body proportions and its relationship to ecology have not been systematically quantified. Using whole-body skeletal models of 410 extinct and extant tetrapods, we show that allometric relationships vary across individual body segments thereby yielding changes in overall body shape as size increases. However, we also find statistical support for quadratic relationships indicative of differential scaling in small-medium versus large animals. Comparisons of locomotor and dietary groups highlight key differences in body proportions that may mechanistically underlie occupation of major ecological niches. Our results emphasise the pivotal role of body proportions in the broad-scale ecological diversity of tetrapods.
... In pythons, another reptile clade showing extreme body size disparity [10], heterochrony also seems to be responsible for morphological divergence at shallower scales, changes in the angle and length of slopes are more common at deeper scales, and significant intercept differences are uncommon. Heterochrony has probably played a central role in some remarkable evolutionary transitions, such as the evolution of the avian and human skulls [15,43]. Previous studies with limited sampling of taxa and traits have shown that heterochrony in Varanidae explains growth patterns [44], sexual dimorphism [45], and the huge size of the extinct V. priscus [46]. ...
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Background Heterochrony, change in the rate or timing of development, is thought to be one of the main drivers of morphological evolution, and allometry, trait scaling patterns imposed by size, is traditionally thought to represent an evolutionary constraint. However, recent studies suggest that the ontogenetic allometric trajectories describing how organisms change as they grow may be labile and adaptive. Here we investigated the role of postnatal ontogenetic development in the morphological diversification of Paleoanguimorpha, the monitor lizards and allies, a clade with extreme body size disparity. We obtained linear and geometric morphometric data for more than 1,600 specimens belonging to three families and 60 species, representing ~ 72% of extant paleoanguimorph diversity. We used these data to undertake one of the largest comparative studies of ontogenetic allometry to date. Results Heterochrony is likely dictating morphological divergence at shallow evolutionary scales, while changes in the magnitude and direction of ontogenetic change are found mainly between major clades. Some patterns of ontogenetic variation and morphological disparity appear to reflect ontogenetic transitions in habitat use. Generally, juveniles are more similar to each other than adults, possibly because species that differ in ecology as adults are arboreal as juveniles. The magnitude of ontogenetic change follows evolutionary models where variation is constrained around an optimal value. Conversely, the direction of ontogenetic change may follow models with different adaptive optima per habitat use category or models where interspecific interactions influence its evolution. Finally, we found that the evolutionary rates of the ontogenetic allometric trajectories are phylogenetically variable. Conclusions The attributes of ontogenetic allometric trajectories and their evolutionary rates are phylogenetically heterogeneous in Paleoanguimorpha. Both allometric constraints and ecological factors have shaped ontogeny in the group. Our study highlights the evolutionary lability and adaptability of postnatal ontogeny, and teases apart how different evolutionary shifts in ontogeny contribute to the generation of morphological diversity at different evolutionary scales.
... The evolution of these features can also be linked with the fact that the nonavian dinosaur/bird transition has been shown to be steplike, mosaic and progressive through time. Birds have evolved many developmental heterochronies over time compared to their nonavian relatives in morphological characters (e.g., Bhullar et al. 2012), and have experienced significant body size and genome size reduction that have been shown to be linked with the evolution of powered flight (Kapusta et al. 2017). However, these morphoecological changes have been shown to have arisen from continuing rapid rates of evolution originating in the deep adaptive radiation of nonavian dinosaurs (e.g., Benson et al. 2014). ...
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Little is known about the large‐scale evolutionary patterns of skull size relative to body size, and the possible drivers behind these patterns, in Archosauromorpha. For example, the large skulls of erythrosuchids, a group of non‐archosaurian archosauromorphs from the Early and Middle Triassic, and of theropod dinosaurs are regarded as convergent adaptations for hypercarnivory. However, few investigations have explicitly tested whether erythrosuchid and theropod skulls are indeed disproportionately large for their body size, and whether this trend is driven by hypercarnivory. Here, we investigate archosauromorph relative skull size evolution, examining the scaling relationships between skull and body size of Palaeozoic and Mesozoic archosauromorphs using a robust phylogenetic framework and assessing the influence of potential drivers, such as taxonomy, diet, locomotory mode and inhabited biotope. Our results show that archosauromorph relative skull sizes are largely determined by phylogeny and that the other drivers have much weaker levels of influence. We find negative allometric scaling of skull size with respect to body size when all studied archosauromorphs are analysed. Within specific groups, skull size scales with positive allometry in non‐archosaurian archosauromorphs and, interestingly, scales isometrically in theropods. Ancestral reconstructions of skull–femur size ratio reveal a disproportionately large skull at the base of Erythrosuchidae and proportionately sized skulls at the bases of Theropoda, Carnosauria and Tyrannosauroidea. Relative skull sizes of erythrosuchids and theropods are therefore distinct from each other, indicating that disproportionately large skulls are not a prerequisite for hypercarnivory in archosauromorphs, and that erythrosuchids exhibit a bauplan unique among terrestrial Mesozoic carnivores.
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Faxinalipterus minimus was originally described as a purported pterosaur from the Late Triassic (early Norian) Caturrita Formation of southern Brazil. Its holotype comprises fragmentary postcranial elements, whereas a partial maxilla was referred to the species. The assignment of Faxinalipterus minimus to Pterosauria has been questioned by some studies, but the specimen has never been accessed in detail after its original description. Here we provide a reassessment of Faxinalipterus minimus after additional mechanical preparation of the holotype. Our interpretations on the identity of several bones differ from those of the original description, and we found no support favoring pterosaur affinities for the taxon. The maxilla previously referred to Faxinalipterus minimus is disassociated from this taxon and referred to a new putative pterosauromorph described here from a partial skull and fragmentary postcranial elements. Maehary bonapartei gen. et sp. nov. comes from the same fossiliferous site that yielded Faxinalipterus minimus, but the lack of overlapping bones hampers comparisons between the two taxa. Our phylogenetic analysis places Faxinalipterus minimus within Lagerpetidae and Maehary bonapartei gen. et sp. nov. as the earliest-diverging member of Pterosauromorpha. Furthermore, the peculiar morphology of the new taxon reveals a new dental morphotype for archosaurs, characterized by conical, unserrated crowns, with a pair of apicobasally oriented grooves. These two enigmatic archosaurs expand our knowledge on the Caturrita Formation fauna and reinforce the importance of its beds on the understanding of Late Triassic ecosystems.
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Heterochrony, defined as a change in the timing of developmental events altering the course of evolution, was first recognized by Ernst Haeckel in 1866. Haeckel's original definition was meant to explain the observed parallels between ontogeny and phylogeny, but the interpretation of his work became a source of controversy over time. Heterochrony took its modern meaning following the now classical work in the 1970–80s by Steven J. Gould, Pere Alberch, and co-workers. Predicted and described heterochronic scenarios emphasize the many ways in which developmental changes can influence evolution. However, while important examples of heterochrony detected with comparative morphological methods have multiplied, the more mechanistic understanding of this phenomenon lagged conspicuously behind. Considering the rapid progress in imaging and molecular tools available now for developmental biologists, this review aims to stress the need to take heterochrony research to the next level. It is time to synchronize the different levels of heterochrony research into a single analysis flow: from studies on organismal-level morphology to cells to molecules and genes, using complementary techniques. To illustrate how to achieve a more comprehensive understanding of phyletic morphological diversification associated with heterochrony, we discuss several recent case studies at various phylogenetic scales that combine morphological, cellular, and molecular analyses. Such a synergistic approach offers to more fully integrate phylogenetic and ontogenetic dimensions of the fascinating evolutionary phenomenon of heterochrony. Highlights • Heterochrony research focuses on comparative morphology but lags on mechanistic understanding. • We propose integrating the different levels of study into a single analysis flow: from morphology to cells to molecules and genes, using modern techniques.
Chapter
Our understanding of the early evolution of birds has advanced over the past 2 decades, thanks to an ever-improving fossil record. Extraordinary fossils have revealed new details about the evolution of the avian brain, respiratory system, digestive tract, and reproductive system. Many of the traits most strongly associated with birds first arose in nonavian theropod dinosaurs. Theropods evolved pennaceous feathers, incipient wings, and gliding flight long before modern birds appeared. Birds likewise inherited features such as an expanded forebrain, gizzard, dorsally immobile lung, pigmented eggs, and paternal brooding system from their theropod ancestors. Yet, the earliest birds also retained primitive traits such as teeth, clawed hands, long bony tails, partially buried nests, and slower growth. The evolution of birds was profoundly influence by the Cretaceous–Paleogene mass extinction, which wiped out the previously dominant Enantiornithines (“opposite birds”). This sets the stage for modern birds to radiate into the most diverse major clade of tetrapods.
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