Spatiotemporal reorganization of growth rates in the evolution of ontogeny

Abstract. Heterochrony, evolutionary changes in rate or timing of development producing parallelism between ontogeny and phylogeny, is viewed as the most common type of evolutionary change in development. Alternative hypotheses such as heterotopy, evolutionary change in the spatial patterning of development, are rarely entertained. We examine the evidence for heterochrony and heterotopy in the evolution of body shape in two clades of piranhas. One of these is the sole case of heterochrony previously reported in the group; the others were previously interpreted as cases of heterotopy. To compare ontogenies of shape, we computed ontogenetic trajectories of shape by multivariate regression of geometric shape variables (i.e., partial warp scores and shape coordinates) on centroid size. Rates of development relative to developmental age and angles between the trajectories were compared statistically. We found a significant difference in developmental rate between species of Serrasalmus , suggesting that heterochrony is a partial explanation for the evolution of body shape, but we also found a significant difference between their ontogenetic transformations; the direction of the difference between them suggests that heterotopy also plays a role in this group. In Pygocentrus we found no difference in developmental rate among species, but we did find a difference in the ontogenies, suggesting that heterotopy, but not heterochrony, is the developmental basis for shape diversification in this group. The prevalence of heterotopy as a source of evolutionary novelty remains largely unexplored and will not become clear until the search for developmental explanations looks beyond heterochrony.     

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.     

Heterochrony and allometry: the analysis of evolutionary change in ontogeny

The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.     

Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae)

Comparative studies of chondrocranial morphology in larval anurans are typically qualitative in nature, focusing primarily on discrete variation or gross differences in the size or shape of individual structures. Detailed data on chondrocranial allometry are currently limited to only two species, Rana sylvatica and Bufo americanus. This study uses geometric morphometric and multivariate statistical analyses to examine interspecific variation in both larval chondrocranial shape and patterns of ontogenetic allometry among six species of Rana. Variation is interpreted within the context of hypothesized phylogenetic relationships among these species. Canonical variates analyses of geometric morphometric datasets indicate that species can be clearly discriminated based on chondrocranial shape, even when whole ontogenies are included in the analysis. Ordinations and cluster analyses based on chondrocranial shape data indicate the presence of three primary groupings (R. sylvatica; R. catesbeiana + R. clamitans; and R. palustris + R. pipiens + R. sphenocephala), and patterns of similarity closely reflect phylogenetic relationships. Analysis of chondrocranial allometry reveals that some patterns are conserved across all species (e.g., most measurements scale with negative allometry, those associated with the posterior palatoquadrate tend to scale with isometry or positive allometry). Ontogenetic scaling along similar allometric trajectories, lateral transpositions of individual trajectories, and variable allometric relationships all contribute to shape differences among species. Overall patterns of similarity among ontogenetic trajectories also strongly reflect phylogenetic relationships. Thus, this study demonstrates a tight link between ontogeny, phylogeny, and morphology, and highlights the importance of including both ontogenetic and phylogenetic data in studies of chondrocranial evolution in larval anurans.     

The role of ontogeny in wood diversity and evolution

Evolutionary developmental biology (evo-devo) explores the link between developmental patterning and phenotypic change through evolutionary time. In this review, we highlight the scientific advancements in understanding xylem evolution afforded by the evo-devo approach, opportunities for further engagement, and future research directions for the field. We review evidence that (1) heterochrony—the change in rate and timing of developmental events, (2) homeosis—the ontogenetic replacement of features, (3) heterometry—the change in quantity of a feature, (4) exaptation—the co-opting and repurposing of an ancestral feature, (5) the interplay between developmental and capacity constraints, and (6) novelty—the emergence of a novel feature, have all contributed to generating the diversity of woods. We present opportunities for future research engagement, which combine wood ontogeny within the context of robust phylogenetic hypotheses, and molecular biology.     

Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles

Snakes possess a derived anatomy, characterized by limb reduction and reorganization of the skull and internal organs. To understand the origin of snakes from an ontogenetic point of view, we conducted comprehensive investigations on the timing of skeletal elements, based on published and new data, and reconstructed the evolution of the ossification sequence among squamates. We included for the first time Varanus, a critical taxon in phylogenetic context. There is comprehensive delay in the onset of ossification of most skeletal elements in snakes when compared to reference developmental events through evolution. We hypothesize that progressing deceleration accompanied limb reduction and reorganization of the snake skull. Molecular and morphological studies have suggested close relationship of snakes to either amphisbaenians, scincids, geckos, iguanids, or varanids. Likewise, alternative hypotheses on habitat for stem snakes have been postulated. Our comprehensive heterochrony analyses detected developmental shifts in ossification for each hypothesis of snake origin. Moreover, we show that reconstruction of ancestral developmental sequences is a valuable tool to understand ontogenetic mechanisms associated with major evolutionary changes and test homology hypotheses. The “supratemporal” of snakes could be homolog to squamosal of other squamates, which starts ossification early to become relatively large in snakes.     

Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six <Emphasis Type="Italic">Triturus</Emphasis> species (Amphibia,Salamandridae)

As with many other amphibians, Triturus species are characterized by a biphasic life cycle with abrupt changes in the cranial skeleton during metamorphosis. The post-metamorphic shape changes of the cranial skeleton were investigated using geometric morphometric techniques in six species: Triturus alpestris, T. vulgaris, T. dobrogicus, T. cristatus, T. carnifex, and T. karelinii. The comparative analysis of ontogenetic trajectories revealed that these species have a conserved developmental rate with divergent ontogenetic trajectories of the ventral skull shape that mainly reflect phylogenetic relatedness. A striking exception in the ontogenetic pattern was possibly found in T. dobrogicus, characterized by a marked increase in the developmental rate compared to the other newt species. The size-related shape changes explained a large proportion of shape change during post-metamorphic growth within each species, with marked positive allometric growth of skull elements related to foraging.     

Ontogenies in mice selected for high voluntary wheel-running activity. I. Mean ontogenies

The evolutionary importance of postnatal ontogenies has long been recognized, but most studies of ontogenetic trajectories have focused exclusively on morphological traits. For animals, this represents a major omission because behavioral traits and their ontogenies often have relatively direct relationships to fitness. Here four replicate lines of house mice artificially selected for high early-age wheel running and their four replicate control lines were used to evaluate the effects of early-age directional selection, genetic drift, and activity environment (presence or absence of a running wheel) on variation in the ontogenies of three traits known to be genetically correlated: voluntary wheel running, body mass, and food consumption. Early-age selection significantly changed both the shape and position of the wheel-running and food-consumption ontogenies while influencing the position, but not the shape, of the body mass ontogeny. Genetic drift (as indicated by variation among replicate lines) produced significant changes in both the position and shape of all three ontogenies; however, its effect differed between the selection and control groups. For wheel running and food consumption, genetic drift only influenced the control ontogenies, whereas for body mass, genetic drift had a significant effect in both selection groups. Both body-mass and food-consumption ontogenies were significantly altered by activity environment, with the environment causing significant changes in the shape and position of both ontogenies. Overall the results demonstrate strong effects of early-age selection, genetic drift, and environmental variation on the evolution and expression of behavioral and morphological ontogenies, with selection changing only the position of the morphological ontogeny but both the position and shape of the behavioral ontogenies.     

Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.     

Heterochrony, maternal effects, and phenotypic variation among sympatric pupfishes

Variation in ontogeny can produce phenotypic variation both within and among species. I investigated whether changes in timing and rate of growth were a source of phenotypic variation in a putative incipient species group of pupfish (Cyprinodon spp.). On San Salvador Island, Bahamas, sympatric forms of pupfish differ in morphology but show only partial reproductive isolation in the laboratory. Offspring from two forms and two geographical areas and their hybrids were bred in the laboratory, and ontogenetic trajectories of their feeding morphology were followed until maturity. In the Bahamian pupfish the two forms grow along similar size but not shape trajectories. Two heterochronic parameters, onset and rate of growth, alter shape trajectories in the Bahamian pupfish. Similar forms from different geographical areas (Florida and the Bahamas) grow along parallel shape trajectories, differing only in one heterochronic parameter, the onset shape. Hybrids within and between the pupfish forms produced intermediate feeding morphologies that were influenced by their maternal phenotype, suggesting that maternal effects may be a source of phenotypic variation in shape that can persist to maturity. In Cyprinodon, small changes in multiple heterochronic parameters translate into large phenotypic differences in feeding morphology.     

Disparate Postnatal Ontogenies Do Not Add to the Shape Disparity of Infants

Integrating studies of ontogeny with analyses of disparity can reveal important and surprising insights into the origins of disparity and why it varies among groups. One such potentially surprising insight is that disparity could be constant over ontogeny even though species differ in both rates and timings of development and in their ontogenetic changes in shape. Several studies of both primates and rodents have concluded that disparity is generated prenatally although some have concluded that it arises postnatally. However, neither constancy nor an ontogenetic increase in disparity has been ever been rigorously documented for either primates or rodents. For a small sample of rodents, we show that species differ in their postnatal ontogenies but infants are neither more nor less disparate than adults and the major dimensions of disparity distinguishing the main clades also do not change. The constancy in both the level of disparity and its main dimensions does not result primarily from the subtlety of postnatal differences. Those differences are indeed subtle but the disparity in directions of ontogenetic shape change is nonetheless sufficient to increase shape disparity significantly. Disparity does not increase postnatally primarily because ontogenies are not strictly linear; disparity generated postnatally counteracts that produced earlier. What limits the progressive accumulation of disparity is the curvature of ontogenetic trajectories, a curvature presumably due to ontogenetic changes in the spatial distribution of rates of bone deposition and resorption.     

The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics

The degree to which the ontogeny of organisms could facilitate our understanding of phylogenetic relationships has long been a subject of contention in evolutionary biology. The famed notion that ‘ontogeny recapitulates phylogeny’ has been largely discredited, but there remains an expectation that closely related organisms undergo similar morphological transformations throughout ontogeny. To test this assumption, we used three‐dimensional geometric morphometric methods to characterize the cranial morphology of 10 extant crocodylian species and construct allometric trajectories that model the post‐natal ontogenetic shape changes. Using time‐calibrated molecular and morphological trees, we employed a suite of comparative phylogenetic methods to assess the extent of phylogenetic signal in these trajectories. All analyses largely demonstrated a lack of significant phylogenetic signal, indicating that ontogenetic shape changes contain little phylogenetic information. Notably, some Mantel tests yielded marginally significant results when analysed with the morphological tree, which suggest that the underlying signal in these trajectories is correlated with similarities in the adult cranial morphology. However, despite these instances, all other analyses, including more powerful tests for phylogenetic signal, recovered statistical and visual evidence against the assumption that similarities in ontogenetic shape changes are commensurate with phylogenetic relatedness and thus bring into question the efficacy of using allometric trajectories for phylogenetic inference.     

Simultaneously mapping and superimposing landmark configurations with parsimony as optimality criterion

All methods proposed to date for mapping landmark configurations on a phylogenetic tree start from an alignment generated by methods that make no use of phylogenetic information, usually by superimposing all configurations against a consensus configuration. In order to properly interpret differences between landmark configurations along the tree as changes in shape, the metric chosen to define the ancestral assignments should also form the basis to superimpose the configurations. Thus, we present here a method that merges both steps, map and align, into a single procedure that (for the given tree) produces a multiple alignment and ancestral assignments such that the sum of the Euclidean distances between the corresponding landmarks along tree nodes is minimized. This approach is an extension of the method proposed by Catalano et al. (2010. Phylogenetic morphometrics (I): the use of landmark data in a phylogenetic framework. Cladistics. 26:539-549) for mapping landmark data with parsimony as optimality criterion. In the context of phylogenetics, this method allows maximizing the degree to which similarity in landmark positions can be accounted for by common ancestry. In the context of morphometrics, this approach guarantees (heuristics aside) that all the transformations inferred on the tree represent changes in shape. The performance of the method was evaluated on different data sets, indicating that the method produces marked improvements in tree score (up to 5% compared with generalized superimpositions, up to 11% compared with ordinary superimpositions). These empirical results stress the importance of incorporating the phylogenetic information into the alignment step.     

Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.     

Phylogenetic interpretation of ontogenetic change: sorting out the actual and artefactual in an empirical case study of centrarchid fishes

Hypothesized relationships between ontogenetic and phylogenetic change in morphological characters were empirically tested in centrarchid fishes by comparing observed patterns of character development with patterns of character evolution as inferred from a representative phylogenetic hypothesis. This phylogeny was based on 56–61 morphological characters that were polarized by outgroup comparison. Through these comparisons, evolutionary changes in character ontogeny were categorized in one of eight classes (terminal addition, terminal deletion, terminal substitution, non-terminal addition, non-terminal deletion, non-terminal substitution, ontogenetic reversal and substitution). The relative frequencies of each of these classes provided an empirical basis from which assumptions underlying hypothesized relationships between ontogeny and phylogeny were tested. In order to test hypothesized relationships between ontogeny and phylogeny that involve assumptions about the relative frequencies of terminal change (e.g. the use of ontogeny as a homology criterion), two additional phylogenies were generated in which terminal addition and terminal deletion were maximized and minimized for all characters. Character state change interpreted from these phylogenies thus represents the maxima and minima of the frequency range of terminal addition and terminal deletion for the 8.7 × 10³⁶ trees possible for centrarchids. It was found for these data that terminal change accounts for c. 75% of the character state change. This suggests either that early ontogeny is conserved in evolution or that interpretation and classification of evolutionary changes in ontogeny is biased in part by the way that characters are recognized, delimited and coded. It was found that ontogenetic interpretation is influenced by two levels of homology decision: an initial decision involving delimitation of the character (the ontogenetic sequence), and the subsequent recognition of homologous components of developmental sequences. Recognition of phylogenetic homology among individual components of developmental sequences is necessary for interpretation of evolutionary changes in ontogeny as either terminal or non-terminal. If development is the primary criterion applied in recognizing individual homologies among parts of ontogenetic sequences, the only possible interpretation of phylogenetic differences is that of terminal change. If homologies of the components cannot be ascertained, recognition of the homology of the developmental sequence as a whole will result in the interpretation of evolutionary differences as substitutions. Particularly when the objective of a study is to discover how ontogeny has evolved, criteria in addition to ontogeny must be used to recognize homology. Interpretation is also dependent upon delimitation within an ontogenetic sequence. This is in part a function of the way that an investigator ‘sees’ and codes characters. Binary and multistate characters influence interpretation differently and predictably. The use of ontogeny for determining phylogenetic polarity as previously proposed rests on the assumptions that ancestral ontogenies are conserved and that character evolution occurs predominantly through terminal addition. It was found for these data that terminal addition may comprise a maximum of 51.9% of the total character state change. It is concluded that the ontogenetic criterion is not a reliable indicator of phylogenetic polarity. Process and pattern data are collected simultaneously by those engaged in comparative morphological studies of development. The set of alternative explanatory processes is limited in the process of observing development. These form necessary starting points for the research of developmental biologists. Separating ‘empirical’ results from interpretational influences requires awareness of potential biases in the course of character selection, coding and interpretation. Consideration of the interpretational problems involved in identifying and classifying phylogenetic changes in ontogeny leads to a re-evaluation of the purpose, usefulness and information conveyed by the current classification system. It is recommended that alternative classification schemes be pursued.     

Heterochronic detection through a function for the ontogenetic variation of bone shape

Heterochrony, evolutionary modifications in the rates and/or the timing of development, is widely recognized as an important agent of evolutionary change. In this paper, we are concerned with the detection of this evolutionary mechanism through the analysis of long bone growth. For this, we provide a function sigma (t) for the ontogenetic variation of bone shape by taking the ratio of two Gompertz curves explaining, respectively, the relative contribution to long bone growth of (a) endochondral ossification and (b) periosteal ossification. The significance of the fitting of this function to empirical data was tested in Anas platyrhynchos (Anseriformes). In this function sigma (t), the time t(m) at which periosteal growth rate first equalizes endochondral growth rate was taken as the timing parameter to be compared between taxa. On the other hand, the maximum rate of ontogenetic change in bone shape (maximum slope, beta) from hatching to t(m) was taken as the rate parameter to be compared. Comparisons of these parameters between the plesiomorphic condition and the derived character state would provide evidence for hypomorphosis (earlier occurrence of t(m)), hyper-morphosis (delayed occurrence of t(m)), deceleration (smaller beta) or acceleration (higher beta).Regarding the phylogenetic context, the ancestral condition for the character of interest should be estimated to polarize the direction of the heterochronic change. We have quantified the influence of the phylogenetic history on the variation of adult bone shape in a sample of 13 species of Anseriformes and 17 species from other neornithine orders of birds by using permutational phylogenetic regressions. Phylogenetic effects are significant, and this fact allows the optimization of bone shape onto a phylogenetic tree of Anseriformes to estimate the ancestral condition for Anas platyrhynchos.     

A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.     

Historical Patterns of Developmental Integration in Piranhas

TO test the hypothesis that developmental integration coordinatesevolutionary change through history, we dissect the spatialand temporal integration of ontogenetic allometries of piranhabody form and examine the evolutionary coordination among ontogeneticfeatures by a phylogenetic analysis. Few of our characters provideevidence in support of the hypothesis. In general, we find thatdevelopmental integration is historically labile, being modifiedat virtually every speciation event. Most of the ontogeneticfeatures are dissociated in their phylogenetic changes and evolvein a mosaic fashion. Indeed, developmental integration is solabile that primitively integrated features of ontogeny usuallyevolve subsequently as independent characters. Evolutionarychanges in developmental integration can result in increasedor decreased integration on the ontogenetic time scale. Whenlocalized features are deleted from ontogeny, or when spatiallyintegrated features are gained, the derived ontogenies may bemore integrated in a spatial sense. The end result of phylogeneticdissociations may be a more highly developmentally integratedontogeny. Thus, in the piranhas we studied, we find a historicallycoupled increase in developmental integration caudally and adecrease indevelopmental integration cranially.     

INTEGRATING DEVELOPMENTAL EVOLUTIONARY PATTERNS AND MECHANISMS: A CASE STUDY USING THE GASTROPOD RADULA

Determining the connection between ontogeny and phylogeny continues to be a major theme in biology. However, few studies have combined dissection of pattern and process that lead to transformation of complex morphological structures. Here we examine the patterns and processes of shape change in a model system—the gastropod radula. This system is a simple one having only two processes: initial secretion and postsecretional movement of teeth. However, it produces a tremendous amount of shape variability and fusion patterns. To determine both pattern and mechanism of shape change in an evolutionary context, we use three complementary approaches and datasets. First, we use a phylogenetic hypothesis to determine the polarity of developmental events. Second, we perform a morphometric analysis of shape change using relative warp analysis that allows us to locate and compare the direction and magnitude of ontogenetic and phylogenetic shape divergence. These comparisons are the basis for testing hyptheses of heterochrony and heterotopy, and we show how our results do not conform to expectations of pure heterochrony. The rejection of heterochrony as a hypothesis is based on empirically demonstrating (1) initial shape differs in each taxon; (2) a single dimension of shape variability does not simultaneously describe ontogenetic and evolutionary shape changes; and (3) a significantly different shape and size covariance between taxa. This rejection is probably based on spatial changes in initial conditions and not spatial changes caused by the process itself. Finally, we construct a mechanistic model that explains how shape change happens based on the sequence of events during ontogeny. By using the parameters in the model as characters in the phylogenetic dataset, we show that different parts of the system have arisen at different times and become co-opted into the process. By integrating our analyses together we show that spatial process parameters can be responsible for our nonspatial patterns and that different ontogenetic processes can create similar end morphologies.