Heterochronic Changes Research Articles

Three modes of heterochrony explain lobule diversity inRadulasubgenusCladoradula(Porellales: Jungermanniopsida), a small lineage of early land plants today

Changes in lobule morphology in Radula subgenus Cladoradula show liverworts have the capacity for dramatic, relatively rapid morphological change by heterochrony. In individuals of R. bipinnata, R. boryana and R. tenax, lobules on secondary and tertiary shoots are progenetic with respect to lobules on primary shoots, in that the slope of the relationship between growth duration and shape does not change. However, in R. campanigera, lobules on secondary and tertiary branches exhibit different slopes from primary branches, but have the same growth duration, a pattern consistent with neoteny. The trajectory of allometric growth is extended or truncated in different species compared with outgroup and ancestral nodes. Changes in duration of lobule growth explain 85% of variation in lobule shape between species. Species are related by relatively shallow nodes in the crown of the Radula subgenus Cladoradula clade, suggesting that divergence and associated heterochronic changes have occurred relatively recently. The rapid morphological diversification in the crown contrasts with the relative stasis between the ancestral node and R. brunnea, the outgroup used in this analysis. A robust primary axis may be required to hold shoots away from vertical surfaces to maximize light interception, and hypermorphosis in lobule ontogeny could be a by-product of the longer growth durations required to build axes sufficiently large to perform this structural role. Alternatively, the large auriculate lobules could function in external water transport systems by providing continuity of surfaces for solute transport via capillary action. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 153–175.

Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species

A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.

Patterns and implications of extensive heterochrony in carnivoran cranial suture closure

Heterochronic changes in the rate or timing of development underpin many evolutionary transformations. In particular, the onset and rate of bone development have been the focus of many studies across large clades. In contrast, the termination of bone growth, as estimated by suture closure, has been studied far less frequently, although a few recent studies have shown this to represent a variable, although poorly understood, aspect of developmental evolution. Here, we examine suture closure patterns across 25 species of carnivoran mammals, ranging from social-insectivores to hypercarnivores, to assess variation in suture closure across taxa, identify heterochronic shifts in a phylogenetic framework and elucidate the relationship between suture closure timing and ecology. Our results show that heterochronic shifts in suture closure are widespread across Carnivora, with several shifts identified for most major clades. Carnivorans differ from patterns identified for other mammalian clades in showing high variability of palatal suture closure, no correlation between size and level of suture closure, and little phylogenetic signal outside of musteloids. Results further suggest a strong influence of feeding ecology on suture closure pattern. Most of the species with high numbers of heterochronic shifts, such as the walrus and the aardwolf, feed on invertebrates, and these taxa also showed high frequency of closure of the mandibular symphysis, a state that is relatively rare among mammals. Overall, caniforms displayed more heterochronic shifts than feliforms, suggesting that evolutionary changes in suture closure may reflect the lower diversity of cranial morphology in feliforms.

Late embryos and bony skull development in Bothropoides jararaca (Serpentes, Viperidae)

In recent years, developmental anatomy received increasing interest as a potential new source for phylogenetic research. For skeletal development, studies mainly rely on the first appearance of ossification centers. However, informative events occur during the whole course of skeletogenesis; interactions between external and internal development occur and morphometric changes take place – all of which present potential sources for phylogenetic analyses. Therefore, the Standard Event System (SES) was used to traceably describe the external development of the snake species Bothropoides jararaca and external measurements were analyzed. We then applied micro-computed tomography (μCT), clearing and double-staining, and 2D and 3D morphometric methods to describe, illustrate, and analyze the development of the head in great detail. We found a 3D flattening of the skull during ontogeny, a pattern that is not reflected in external development. This may be explained by a different relationship of skeletogenesis and external characters to the developing jaw musculature or simply by the different type of data. Clearing and double-staining and μCT-scanning revealed a broadly similar sequence in the onset of ossification. Minute differences may be due to the treatment of embryos. Bones of the dermatocranium are among the first to ossify and the development of the calcified endolymph may reflect its function as a calcium source during development. The value of phylogenetic observations using the sequence of first ossifications is critically discussed. The related heterochronic changes are interpreted to contribute at least to the very first phase of divagating skull formation among taxa.

Transcriptional evolution underlying vertebrate sexual development

Explaining the diversity of vertebrate sex-determining mechanisms ranging from genotypic (GSD) to temperature-dependent (TSD) remains a developmental and evolutionary conundrum. Using a phylogenetic framework, we explore the transcriptional evolution during gonadogenesis of several genes involved in sexual development, combining novel data from Chrysemys picta turtles (TSD) and published data from other TSD and GSD vertebrates. Our novel C. picta dataset underscores Sf1 and Wt1 as potential activators of the thermosensitive period and uncovered the first evidence of Dax1 involvement in male development in a TSD vertebrate. Contrasting transcriptional profiles revealed male-biased Wt1 expression in fish while monomorphic expression is found in tetrapods but absent in turtles. Sf1 expression appears highly labile with transitions among testicular, ovarian, and non-sex-specific gonadal formation patterns among and within lineages. Dax1's dual role in ovarian and testicular formation is found in fish and mammals but is dosage-sensitive exclusively in eutherian mammals due to its X-linkage in this group. Contrastingly, Sox9 male-biased and Aromatase female-biased expression appear ancestral and virtually conserved throughout vertebrates despite significant heterochronic changes in expression as other elements likely replaced their function in early gonadogenesis. Finally, research avenues are highlighted to further study the evolution of the regulatory network of sexual development.

Osteology and postmetamorphic development of Telmatobius oxycephalus (Anura: Telmatobiidae) with an analysis of skeletal variation in the genus

The osteological diversity among species of Telmatobius has been considered conservative. Nonetheless, the degree of ossification of several features varies both intraspecifically and interspecifically. Herein, intraspecific osteological variation and postmetamorphic ontogenetic changes in osteological features are described in Telmatobius oxycephalus. These data are compared with published descriptions of congeners. There is a considerable intraspecific osteological variation in T. oxycephalus, with cranial characters varying polymorphically, and the hyoid and postcranial characters being sexually dimorphic. This intraspecific variation is expressed by subtle differences in the degree of ossification or mineralization. Interspecific variation also can be described in terms of differential development of osteological features; these differences are more obvious than intraspecifically variable characters. The adult skeletons of several species of Telmatobius resemble the morphology observed in early stages of postmetamorphic development of T. oxycephalus. This is especially evident in the neopalatines, parasphenoid, sphenethmoid, exoccipitals, prootics, vomers, nasals, and plectra. These results suggest that within the conservative osteological architecture of Telmatobius, the variation observed is the result of heterochronic changes during the ossification process.

Mechanisms of Speciation

Mechanisms of Speciation

Functional conservation and divergence of BMP ligands in limb development and lipid homeostasis of holometabolous insects

Bone morphogenetic protein (BMP) ligands play key roles in regulating morphological and physiological traits. To investigate how the functions of BMP ligands have evolved among insects, the roles of two key BMP ligands, decapentaplegic (dpp) and glass bottom boat (gbb), were studied in the flour beetle, Tribolium castaneum. RNA interference-mediated knockdown revealed that the role of dpp in establishing limb segmentation is conserved among insects. Based on the expression pattern of dpp in the presumptive leg tarsal segments, we propose that the function of dpp has evolved through heterochronic changes during the evolution of complete metamorphosis. Gbb1 was found to be necessary for sculpting the tarsal segment morphology characteristic of beetles. Knockdown of Dpp and Gbb1 expression also resulted in transparent larvae and reduced triglyceride levels, indicating their critical roles in maintaining lipid homeostasis. Both knockdown phenotypes were mediated by larval translucida. Because only Gbb regulates lipid metabolism in Drosophila, regulation of lipid homeostasis appears to have evolved by developmental systems drift. Thus, developmental systems drift may underlie evolution of both morphology and physiological processes.

A Phenotypic Point of View of the Adaptive Radiation of Crested Newts (Triturus cristatus Superspecies, Caudata, Amphibia).

The divergence in phenotype and habitat preference within the crested newt Triturus cristatus superspecies, examined across different ontogenetic stages, provides an excellent setting to explore the pattern of adaptive radiation. The crested newts form a well-supported monophyletic clade for which at least the full mitochondrial DNA phylogeny is resolved. Here we summarise studies that explored the variation in morphological (larval and adult body form, limb skeleton, and skull shape) and other phenotypic traits (early life history, developmental sequences, larval growth rate, and sexual dimorphism) to infer the magnitude and direction of evolutionary changes in crested newts. The phenotypic traits show a high level of concordance in the pattern of variation; there is a cline-like variation, from T. dobrogicus, via T. cristatus, T. carnifex, and T. macedonicus to the T. karelinii group. This pattern matches the cline of ecological preferences; T. dobrogicus is relatively aquatic, followed by T. cristatus. T. macedonicus, T. carnifex, and the T. karelinii group are relatively terrestrial. The observed pattern indicates that phenotypic diversification in crested newts emerged due to an evolutionary switch in ecological preferences. Furthermore, the pattern indicates that heterochronic changes, or changes in the timing and rate of development, underlie the observed phenotypic evolutionary diversification.

Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait

Within Anura, direct development involves ontogenetic changes of the biphasic ancestral pattern. The recent partitioning of the genus Eleutherodactylus, along with the proposition of the unranked taxon Terrarana, has renewed an interest to the morphological and ecological diversity among direct-developing frogs. The morphological changes during embryonic development of Oreobates barituensis is similar to those of other Neotropical direct-developing species, including the reduction or absence of several larval and embryonic characters (e.g., external gills and adhesive glands), heterochronic changes (e.g., early developing limbs and late persistence of ciliated epidermal cells), and the appearance of new structures (e.g., egg tooth). The tail achieves an extraordinary peramorphic development (encloses the entire embryo), and the location of its expanded part is interpreted as a heterotopic change resulting in a novel trait. An enveloping tail with apparently non-heterotopic fins, combined with the absence of gills, has been only reported for a species of the related genus Craugastor, and these morphologies suggest an informative perspective for the study of evolution of direct development in terraranans.

Testing gradual and speciational models of evolution in extant taxa: the example of ratites

Ever since Eldredge and Gould proposed their model of punctuated equilibria, evolutionary biologists have debated how often this model is the best description of nature and how important it is compared to the more gradual models of evolution expected from natural selection and the neo-Darwinian paradigm. Recently, Cubo proposed a method to test whether morphological data in extant ratites are more compatible with a gradual or with a speciational model (close to the punctuated equilibrium model). As shown by our simulations, a new method to test the mode of evolution of characters (involving regression of standardized contrasts on their expected standard deviation) is easier to implement and more powerful than the previously proposed method, but the Mesquite module comet (aimed at investigating evolutionary models using comparative data) performs better still. Uncertainties in branch length estimates are probably the largest source of potential error. Cubo hypothesized that heterochronic mechanisms may underlie morphological changes in bone shape during the evolution of ratites. He predicted that the outcome of these changes may be consistent with a speciational model of character evolution because heterochronic changes can be instantaneous in terms of geological time. Analysis of a more extensive data set confirms his prediction despite branch length uncertainties: evolution in ratites has been mostly speciational for shape-related characters. However, it has been mostly gradual for size-related ones.

Causes and consequences of expanded subventricular zones

Primates have evolved an expanded isocortex relative to many other mammals. Parrots and songbirds have evolved an expanded telencephalon relative to many other birds. Previous work suggests that the expansion of the telencephalon in parrots and songbirds as well as the isocortex in primates is achieved, at least in part, by selectively delaying neurogenesis, expanding the subventricular zone (SVZ) and delaying maturation. The finding that similar developmental alterations in the spatial and temporal pattern of neurogenesis evolved together in these two distant lineages suggests that a single change in developmental mechanism might account for the expansion of the isocortex or telencephalon. We here review how uniformly lengthening developmental schedules may result in delays of neurogenesis, the expansion of the SVZ and delayed maturation. We propose that delays in neurogenesis may cause ventricular zone (VZ) cells to proliferate faster than the VZ can expand, which may force many proliferating cells to leave the VZ and form an expanded SVZ. Prolonged proliferation in the VZ and SVZ causes delays in neuronal maturation, which in turn may promote learning from conspecifics. Thus, we suggest that a single heterochronic change in developmental timing may orchestrate a variety of changes in the spatial and temporal pattern of proliferation, which has important behavioral consequences in adulthood.

Morphogenesis and phenotypic divergence in two developmental morphs of Streblospio benedicti (Annelida, Spionidae)

Abstract. The morphology of marine invertebrate larvae is strongly correlated with egg size and larval feeding mode. Planktotrophic larvae typically have suites of morphological traits that support a planktonic, feeding life style, while lecithotrophic larvae often have larger, yolkier bodies, and in some cases, a reduced expression of larval traits. Poecilogonous species provide interesting cases for the analysis of early morphogenesis, as two morphs of larvae are produced by a single species. We compared morphogenesis in planktotrophic and lecithotrophic morphs of the poecilogonous annelid Streblospio benedicti from the trochophore stage through metamorphosis, using observations of individuals that were observed alive, with scanning electron microscopy, or in serial sections. Offspring of alternate developmental morphs of this species are well known to have divergent morphologies in terms of size, yolk content, and the presence of larval bristles. We found that some phenotypic differences between morphs occur as traits that are present in only one morph (e.g., larval bristles, bacillary cells on the prostomium and pygidium), but that much of the phenotypic divergence is based on heterochronic changes in the differentiation of shared traits (e.g., gut and coelom). Tissue and organ development are compared in both morphs in terms of their structure and ontogenetic change throughout early development and metamorphosis.

A large-scale survey of heterochrony in anuran cranial ossification patterns

Most anurans have a biphasic life cycle, which includes metamorphosis from a tadpole stage to an adult frog. This process involves extensive transformations of the cranial skeleton, which have been of long-standing interest with respect to anuran skeletal evolution and taxonomy. In this study, large-scale patterns of anuran skeletal ossification are assessed by collecting the most comprehensive data set on anuran cranial ossification to date from the literature, including data for 45 anuran and one caudate outgroup species. Ossification sequences were translated into event-pair matrices for explorative phylogenetic analysis and phylogenetically informed parsimony search for heterochrony using the Parsimov algorithm. Rank variability of single bones across species was also analysed. Little phylogenetic signal was retrieved from a parsimony-based phylogenetic analysis of event-pairs, and only a few species that are generally agreed to be closely related are placed close to each other (e.g. some Pipidae and Costata). Parsimov analysis revealed some clade-specific heterochrony in anuran clades of varying inclusiveness. Our results show that relating heterochronic changes in anuran cranial ontogeny to parameters such as direct development or miniaturization is problematic because of the high evolvability of cranial ossification sequences. Rank variation analysis suggests that anuran cranial bones are highly variable in their sequence positioning, possibly because tadpole and adult cranial morphology do not co-evolve. Elements which are lost in some species ossify at the end of the sequence, providing evidence for the notion that failure of anuran cranial elements to ossify is due to processes of paedomorphosis. Die meisten Anura (Froschlurche) zeichnen sich durch einen biphasischen Lebenszyklus aus, während dessen sie eine Metamorphose vom Kaulquappenstadium zum adulten Frosch durchlaufen. Die Metamorphose geht mit weitreichenden Umformungen im kraniellen Skelett einher. Dieses Phänomen stößt seit langem im Rahmen von Fragestellungen mit Bezug auf Skelettevolution und taxonomische Klassifizierung auf Interesse. In der vorliegenden Studie werden anhand der bisher umfassendsten Datenerhebung, basierend auf der Literatur der letzten 50 Jahre, die Reihenfolge der Verknöcherung im Kranialskelett der Anura untersucht. Einbezogen wurden kranielle Verknöcherungs-sequenzen von 45 Vertretern der Anura und einem Vertreter der Caudata (Schwanzlurche). Die Sequenzen wurden als ‘Event-pairs’ kodiert, um eine informelle phylogenetische Analyse nach dem Sparsamkeitsprinzip sowie phylogenetisch basierte Heterochronieanalysen unter Anwendung des Parsimov-Algorithmus durchzuführen. Außerdem wurde die zwischenartliche Variabilität des Verknöcherungszeitpunktes innerhalb der Sequenz für die einzelnen Knochen untersucht. Die phylogenetische Analyse gruppierte einige Arten, welche generell als nahverwandt angesehen werden, z.B. einige Vertreter der Pipiden und Costata. Die Parsimov-Analyse zeigte, daß sich nur wenige Anurengruppen unterschiedlicher Diversität durch Heterochronien ausweisen. Unsere Ergebnisse zeigen, dass eine kausale Verbindung von Heterochronien mit Eigenschaften wie Direktentwicklung problematisch ist. Die Analyse der Verknöcherungsvariabilität weist auf große Variabilität des Verknöcherungs-Zeitpunkt der einzelnen Knochen hin; dies kann möglicherweise durch die relativ unabhängige Evolution von Larval- und Adultschädelmorhpologie erklärt werden. Elemente, die in einigen Arten nicht vorkommen, verknöchern generell am Ende der Sequenz. Dies spricht für die Annahme, daß der Verlust von Schädelknochen bei Anuren auf Pädomorphose zurückzuführen ist.

Morphological Evolution of Newly Metamorphosed Sea Urchins—A Phylogenetic and Functional Analysis

Newly metamorphosed juvenile sea urchins are highly variable across taxa. This contribution documents and illustrates structural, functional, and phylogenetic variation among newly metamorphosed juvenile sea urchins for 31 species from 12 ordinal or familial lineages. The classic juvenile with five primary podia, 20 interambulacral spines, and variable numbers of juvenile spines is found commonly among new metamorphs across lineages, but there are many examples, which depart from this pattern and most likely reflect adaptation to settlement habitats. At metamorphosis juveniles can have 5-25 functional podia. They can have 0-65 spines, 0 or 5 sphaeridia (balance organs). They may have zero or up to eight pedicellariae. While competent larvae that delay metamorphosis may continue to develop juvenile structures, variation across species is much greater than within species and there are strong phylogenetic and functional differences among juveniles. Heterochronic changes in expression of these structures can account for differences among taxa. Based on this sample, juvenile characters such as spines, podia, and larval pedicellariae are expressed in ways that suggest they are developmental modules whose expression can be readily changed relative to one another and to the time of metamorphosis.

Differential regulations of wing and ovarian development and heterochronic changes of embryogenesis between morphs in wing polyphenism of the vetch aphid

In wing polyphenisms that produced alternative wing morphs depending on environmental conditions, the developmental regulations to balance between flight and reproductive abilities should be important. Many species of aphids exhibit wing polyphenisms, and the development of wing and flight muscles is thought to incur costs of reproductive ability. To evaluate the relationship between flight and reproduction, the fecundity and the wing- and ovarian development in the parthenogenetic generations were compared between winged and wingless aphids in the vetch aphid Megoura crassicauda. Although no differences in offspring number and size were detected, the onset of larviposition after imaginal molt was delayed in winged adults. The comparison of growth in flight apparatus revealed that, after the second-instar nymphs, the flight-apparatus primordia of presumptive wingless aphids were degenerated while those of winged nymphs rapidly developed. In the ovaries of winged line, the embryo size was smaller and the embryonic stages were delayed from third to fifth instars, although these differences had disappeared by the time of larviposition. It is therefore likely that the delay in larviposition in winged aphids is due to the slower embryonic development. The correlation between embryo size and developmental stage suggests that the embryos of winged aphids are better developed than similarly sized embryos in wingless aphids. These heterochronic shifts would facilitate the rapid onset of larviposition after the dispersal flight. This developmental regulation of embryogenesis in the aphid wing polyphenism is suggested to be an adaptation that compensates the delay of reproduction caused by the wing development.

Earliest ontogeny of Early Palaeozoic Craniiformea: implications for brachiopod phylogeny

Popov, L.E., Bassett, M.G., Holmer, L.E., Skovsted, C.B. & Zuykov, M.A. 2010: Earliest ontogeny of Early Palaeozoic Craniiformea: implications for brachiopod phylogeny. Lethaia, Vol. 43, pp. 323–333. Well preserved specimens of the Early Palaeozoic craniiform brachiopods Orthisocrania and Craniops retain clear evidence of a lecithotrophic larval stage, indicating the loss of planktotrophy early in their phylogeny. The size of the earliest mineralized dorsal shell was <100 μm across, and the well preserved shell structure in these fossil craniiforms allows their earliest ontogeny to be compared directly with that of living Novocrania, in which the first mineralized dorsal shell (metamorphic shell) is secreted only after settlement of the lecithotrophic larvae. Immediately outside this earliest shell (early post-metamorphic or brephic shell) and in the rest of the dorsal valve the primary layer in both fossil and living craniiforms has characteristic radially arranged laths, which are invariably lacking in the earliest dorsal shell. The ventral valve of the fossil specimens commonly preserves traces of an early attachment scar (cicatrix), which is equal in size to the dorsal metamorphic shell, and the brephic post-metamorphic ventral valve also has a primary shell with radially arranged laths. However, a primary shell with radial laths is completely lacking in the ventral valve of living Novocrania, indicating that heterochrony may have been involved in the origin of the encrusting mode of life in living craniids; the entire ventral valve of Recent craniids (with the possible exception of Neoancistrocrania) may correspond to the earliest attachment scar of some fossil taxa such as Orthisocrania. It is also probable that the unique absence of an inner mantle lobe as well as the absence of lobate cells in Novocrania could be the result of heterochronic changes. The dorsal valve of both fossil and living craniiforms has a marked outer growth ring, around 500 μm across, marking the transition to the adult, and a significant change in regime of shell secretion. The earliest craniiform attachment is considered to be homologous to the unique attachment structures described recently in polytoechioids (e.g. Antigonambonites) and other members of the strophomenate clade. However, unlike the craniiforms, polytoechioids and strophomenates all have planktotrophic larvae, and planktotrophy is most probably a plesiomorphic character for all Brachiopoda. □Brachiopoda, Craniiformea, Early Palaeozoic, ontogeny, phylogeny.

The morphology and post-hatching development of the skull of Bolitoglossa nicefori (Caudata: Plethodontidae): developmental implications of recapitulation and repatterning

The cranial morphology of the direct-developing salamander Bolitoglossa nicefori and its post-hatching development are described and compared with that of other urodeles. Four stages of cranial development are defined on the basis of conspicuous events that occur during post-hatching ontogeny. The adult skull morphology of B. nicefori is similar to that of other plethodontids; however, some regions show interspecific variation. The post-hatching ontogeny of the skull and the stage of ossification observed in the hatchlings of B. nicefori show two important ontogenetic features: (1) a mosaic of early larval, metamorphic and post-metamorphic skull features in hatchlings, and (2) absence of characteristic larval elements in skull and hyoid apparatus. The distinctive stage of ossification in the hatchlings of B. nicefori could be caused by heterochronic changes in the ossification sequence, compared to the ontogeny of metamorphic salamanders. The possible heterochronic changes and the absence of larval traits are perhaps due to ontogenetic repatterning, yet without an obvious impact on the adult skull morphology (absence of morphological novelties). This might indicate a compartmentalized development. Further studies should be performed in order to establish the possible occurrence of recapitulatory patterns or ontogenetic repatterning in the skull morphogenesis of B. nicefori during its embryonic development.

Spectacular morphological novelty in a miniature cyprinid fish, Danionella dracula n. sp.

Danionella dracula is a new species of sexually dimorphic, miniature and highly developmentally truncated cyprinid fish. Compared with its close relative, the zebrafish Danio rerio, it lacks 44 bones or parts thereof and represents one of the most developmentally truncated vertebrates. Absence of the majority of bones appears to be due to developmental truncation via terminal deletion. In contrast to these larval-like features, D. dracula also shows several hyperossifications. Uniquely, among carp-like fishes, male D. dracula have a series of long, pointed odontoid processes on the jaws greatly resembling the jaw dentition of teleosts with true teeth. The anterior-most process in each jaw is extended as a canine-like fang projecting through the epithelium. True jaw teeth are absent from all 3700 species of cypriniforms and were lost at least in the Upper Eocene. It remains to be investigated, however, whether the conserved pathways to regulate tooth development in cypriniforms have been used in D. dracula to form and pattern the odontoid processes. This new species represents a remarkable example linking progenetic paedomorphosis via heterochronic change in developmental timing to the evolution of morphological novelties.

Morphological evolution in Ceratophryinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis

Heterochrony produces morphological change with effects in shape, size, and/or timing of developmental events of a trait related to an ancestral ontogeny. This paper analyzes heterochrony during the ontogeny of Ceratophryinae (Ceratophrys, Chacophrys, and Lepidobatrachus), a monophyletic group of South American frogs with larval development, and uses different approaches to explore their morphological evolution: (1) inferences of ancestral ontogenies and heterochronic variation from a cladistic analysis based on 102 morphological larval and adult characters recorded in ten anuran taxa; (2) comparisons of size, morphological variation, and timing (age) of developmental events based on a study of ontogenetic series of ceratophryines, Telmatobius atacamensis, and Pseudis platensis. We found Chacophrys as the basal taxon. Ceratophrys and Lepidobatrachus share most derived larval features resulting from heterochrony. Ceratophryines share high rates of larval development, but differ in rates of postmetamorphic growth. The ontogeny of Lepidobatrachus exhibits peramorphic traits produced by the early onset of metamorphic transformations that are integrated in an unusual larval morphology. This study represents an integrative examination of shape, size, and age variation, and discusses evolutionary patterns of metamorphosis. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 752–780.