Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of the Ardeidae

Evolutionary changes in developmental timing and rates (heterochrony) are a source of morphological variation. Here we explore a central issue in heterochronic analysis: are the alterations in developmental timing and rates the only factor underlying morphological heterochrony? Tarsometatarsal growth through endochondral ossification in Ardeidae evolution has been taken as a case study. Evolutionary changes in bone growth rate (morphological heterochrony) might be either (a) the result of alterations in the mitotic frequency of epiphyseal chondrocytes (process‐heterochrony hypothesis), or (b) the outcome of alterations in the number of proliferating cells or in the size of hypertrophic chondrocytes (structural hypothesis). No correlation was found between tarsometatarsal growth rates and the frequency of cell division. However, bone growth rates were significantly correlated with the number of proliferating cells. These results support the structural hypothesis: morphological acceleration and deceleration are the outcome of evolutionary changes in one structural variable, the number of proliferating cells.     

Larval developmental stages of laboratory-reared silver pomfret,pampus argenteus

Eggs of the silver pomfret,Pampus argenteus, were collected and artificially fertilized by stripping fully-ripe male and female broodstock caught by gillnets in Kuwait waters during June 1997. Larvae hatched from fertilized eggs were reared until 90 days after hatching (DAH) in water temperatures of 27–30°C. Newly-hatched larvae grew from an average of 2.4 mm in body length (BL) to 3.7, 4.4, 7.2 and 8.4 mm at 8, 12, 24 and 30 DAH, respectively. Myomere and vertebral numbers ranged from 34 to 36. Transformation from the larval to juvenile form was completed at 22.2 mm BL (40 DAH). Dorsal and anal fin spines first appeared when juveniles reached 38.8 mm BL (50 DAH). Body depth increased with increase in body length; a rapid increase in body depth occurred in larvae 7.1–8.0 mm, reaching 57% of BL, and further increased to 69% of BL in juveniles 38.8 to 47.9 mm. Pigmentation during development is described and illustrated.     

Larval cannibalism during the late developmental stages of a facultatively gregarious encyrtid endoparasitoid

• 1 The larvae of many gregarious parasitoid species are usually non‐aggressive when they develop in or on a host, but those of Metaphycus flavus are one of the few exceptions known. Herein we describe their aggressive behaviour and the conditions under which it occurs, using observations in which larval development and physical conflict within parasitised and superparasitised hosts were mapped daily.
• 2 Metaphycus flavus larvae often engaged in physical conflict that resulted in consumption of the losing larvae (= cannibalism ) in superparasitised hosts, whereas such conflict and consumption occurred rarely when a single brood developed in a host.
• 3 Cannibalism among M. flavus larvae only occurred after the host resources had become scarce. Typically it occurred after the sixth day of development (fourth‐instar larvae) when the larvae in a clutch had separated from their aeroscopic plate and were freed of their attachment to the host's cuticle.
• 4 Female larvae in the initial clutch appeared more aggressive than male larvae when a second clutch was allocated 4 h after the first clutch. The probability of a larva being attacked and consumed by a brood mate increased as the number of larvae increased in the host. This partial tolerance might allow the members of the initial brood to defend themselves from offspring of a superparasitising female (= competitors ). Such post‐ovipositional regulation of brood size might be interpreted as high‐density intolerance among female offspring.

     

Time's arrow: heterochrony and the evolution of development

The concept of heterochrony, which denotes a change in the relative timing of developmental events and processes in evolution, has accompanied attempts to link evolution and development for well over a century. During this time the definition of heterochrony and the application of the concept have varied and by the late 1990's, many questioned the usefulness of the concept. However, in the past decade studies of heterochrony have been revitalized by a new focus on developmental sequence, an examination of heterochrony in explicit phylogenetic contexts and increasing tendencies to examine the heterochrony of many kinds of events, including cellular, molecular and genetic events. Examples of such studies are reviewed in this paper and it is argued that this new application of heterochrony provides an extraordinarily rich opportunity for understanding the developmental basis of evolutionary change.     

Sequence heterochrony and the evolution of development

One of the most persistent questions in comparative developmental biology concerns whether there are general rules by which ontogeny and phylogeny are related. Answering this question requires conceptual and analytic approaches that allow biologists to examine a wide range of developmental events in well-structured phylogenetic contexts. For evolutionary biologists, one of the most dominant approaches to comparative developmental biology has centered around the concept of heterochrony. However, in recent years the focus of studies of heterochrony largely has been limited to one aspect, changes in size and shape. I argue that this focus has restricted the kinds of questions that have been asked about the patterns of developmental change in phylogeny, which has narrowed our ability to address some of the most fundamental questions about development and evolution. Here I contrast the approaches of growth heterochrony with a broader view of heterochrony that concentrates on changes in developmental sequence. I discuss a general approach to sequence heterochrony and summarize newly emerging methods to analyze a variety of kinds of developmental change in explicit phylogenetic contexts. Finally, I summarize a series of studies on the evolution of development in mammals that use these new approaches.     

Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony

Developmental biology often yields data in a temporal context. Temporal data in phylogenetic systematics has important uses in the field of evolutionary developmental biology and, in general, comparative biology. The evolution of temporal sequences, specifically developmental sequences, has proven difficult to examine due to the highly variable temporal progression of development. Issues concerning the analysis of temporal sequences and problems with current methods of analysis are discussed. We present here an algorithm to infer ancestral temporal sequences, quantify sequence heterochronies, and estimate pseudoreplicate consensus support for sequence changes using Parsimov-based genetic inference [PGi]. Real temporal developmental sequence data sets are used to compare PGi with currently used approaches, and PGi is shown to be the most efficient, accurate, and practical method to examine biological data and infer ancestral states on a phylogeny. The method is also expandable to address further issues in developmental evolution, namely modularity.     

The dentary of hadrosauroid dinosaurs: evolution through heterochrony

The near-global distribution of hadrosaurid dinosaurs during the Cretaceous has been attributed to mastication, a behaviour commonly recognized as a mammalian adaptation. Its occurrence in a non-mammalian lineage should be accompanied by the evolution of several morphological modifications associated with food acquisition and processing. This study investigated morphological variation in the dentary, a major element of the hadrosauroid lower jaw. Eighty-four hadrosauroid dentaries were subjected to geometric morphometric and statistical analyses to investigate their taxonomic, ontogenetic, and individual variation. Results suggest increased food acquisition and processing efficiency in saurolophids through a complex pattern of evolutionary and growth-related changes. The edentulous region grew longer relative to dentary length, allowing for food acquisition specialization anteriorly and processing posteriorly, and became ventrally directed, possibly associated with foraging low-growing vegetation, especially in younger individuals. The saurolophid coronoid process became anteriorly directed and relatively more elongate, with an expanded apex, increasing moment arm length, with muscles pulling the jaw more posteriorly, increasing mechanical advantage. During growth, all hadrosauroids underwent anteroposterior dental battery elongation by the addition of teeth, and edentulous region ventralization decreased. The dental battery became deeper in saurolophids by increasing the number of teeth per tooth family. The increased coronoid process anterior inclination and relative edentulous region elongation in saurolophids are hypothesized to have evolved through hypermorphosis and/or acceleration, peramorphic heterochronic processes; the development of an anteroposteriorly shorter but dorsoventrally taller saurolophid dentary, is probably due to post-displacement in dental battery elongation and edentulous region decreased ventral orientation, a paedomorphic heterochronic process.     

Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid

SUMMARY Biologists measure developmental time by dividing development into arbitrary time blocks called "stages." This is a reasonable approach, provided that developmental timing is precisely controlled within a species. However, the degree of this precision is unknown. This is unfortunate because precision in developmental timing at the population level is a central issue to the whole research program of heterochrony. To examine this issue, we apply Ontogenetic Sequence Analysis to 261 embryos of the Lake Victoria cichlid Haplochromis piceatus . The result of our analysis can be mapped as a complex web of 26,880 equally parsimonious developmental sequences. This topology reflects timing polymorphism (intraspecific heterochrony) among embryos of this species. Because of this timing polymorphism, it is not possible to define discrete "stages" in this cichlid (although there is sufficient sequence signal to assess the maturity of embryos). More generally, we show that sequence polymorphism creates uncertainty about how a given embryo will develop implying that the mechanisms controlling developmental timing in embryos lack precision. For this reason, it is imperative to consider patterns of embryonic variability when measuring developmental time.     

Larval exchange and dispersion of polychaetes between a bay and the ocean

A dynamic meroplanktonic study of the Bay of Arcachon (France)and the nearby continental shelf has been undertaken to examinethe degree of larval exchange between the two ecosystems. ArcachonBay is a bight connected via a narrow strait to the ocean, especiallyrich in invertebrate communities and more particularly polychaetes(>200 species have been indexed). The exchange of water massesbetween the oceanic system and the coastal lagoon is the consequenceof strong tidal currents. Several well-represented species oflarval polychaete populations were used as an index of communication(larval flow) between these systems, and allowed testing ofwhether one of the ecosystems is beneficial to the other. Thisstudy tends to demonstrate that the theory of a larval dispersionfavoured by pelagic life is not necessarily verified.     

Evidence for heterochrony in the cranial evolution of fossil crocodyliforms

The southern supercontinent of Gondwana was home to an extraordinary diversity of stem‐crocodylians (Crocodyliformes) during the Late Cretaceous. The remarkable morphological disparity of notosuchian crocodyliforms indicates that this group filled a wide range of ecological roles more frequently occupied by other vertebrates. Among notosuchians, the distinctive cranial morphology and large body sizes of Baurusuchidae suggest a role as apex predators in ecosystems in which the otherwise dominant predatory theropod dinosaurs were scarce. Large‐bodied crocodyliforms, modern and extinct, are known to have reached large sizes by extending their growth period. In a similar way, peramorphic heterochronic processes may have driven the evolution of the similarly large baurusuchids. To assess the presence of peramorphic processes in the cranial evolution of baurusuchids, we applied a geometric morphometric approach to investigate ontogenetic cranial shape variation in a comprehensive sample of notosuchians. Our results provide quantitative morphological evidence that peramorphic processes influenced the cranial evolution of baurusuchids. After applying size and ancestral ontogenetic allometry corrections to our data, we found no support for the action of either hypermorphosis or acceleration, indicating that these two processes alone cannot explain the shape variation observed in Notosuchia. Nevertheless, the strong link between cranial shape variation and size increase in baurusuchids suggests that peramorphic processes were involved in the emergence of hypercarnivory in these animals. Our findings illustrate the role of heterochrony as a macroevolutionary driver, and stress, once more, the usefulness of geometric morphometric techniques for identifying heterochronic processes behind evolutionary trends.     

Vertebral evolution and ontogenetic allometry: The developmental basis of extreme body shape divergence in microcephalic sea snakes

Snakes exhibit a diverse array of body shapes despite their characteristically simplified morphology. The most extreme shape changes along the precloacal axis are seen in fully aquatic sea snakes (Hydrophiinae): “microcephalic” sea snakes have tiny heads and dramatically reduced forebody girths that can be less than a third of the hindbody girth. This morphology has evolved repeatedly in sea snakes that specialize in hunting eels in burrows, but its developmental basis has not previously been examined. Here, we infer the developmental mechanisms underlying body shape changes in sea snakes by examining evolutionary patterns of changes in vertebral number and postnatal ontogenetic growth. Our results show that microcephalic species develop their characteristic shape via changes in both the embryonic and postnatal stages. Ontogenetic changes cause the hindbodies of microcephalic species to reach greater sizes relative to their forebodies in adulthood, suggesting heterochronic shifts that may be linked to homeotic effects (axial regionalization). However, microcephalic species also have greater numbers of vertebrae, especially in their forebodies, indicating that somitogenetic effects also contribute to evolutionary changes in body shape. Our findings highlight sea snakes as an excellent system for studying the development of segment number and regional identity in the snake precloacal axial skeleton.     

The ontogenetic complexity of developmental constraints

Developmental constraint is a theoretically important construct bridging ontogenetic and evolutionary studies. We propose a new operationalization of this notion that exploits the unusually rich measurement structure of landmark data. We represent landmark configurations by their partial warps, a basis for morphospace that represents a set of localized features of form. A finding of developmental constraint arises from the interplay between age-varying means and age-specific variances in these subspaces of morphospace. Examination of variances and means in 16 ventral skull landmarks in the cotton rat S. fulviventer at ages 1, 10, 20, and 30 days yielded three types of developmental constraint: canalization (constraint to relatively constant form age by age); chreods (reduction of variance orthogonal to the mean trajectory over ages); and opposition (reduction of age-specific variance along the mean trajectory over ages). While canalization and chreodic constraints have been noted previously, the oppositional type of constraint appears novel. Only one of our characters, relative length and orientation of the incisive foramen, appears to be canalized. Although skull growth becomes increasingly integrated through ontogeny, our characters display a remarkable spatiotemporal complexity in patterns of variance reduction. The specific assortment of constraints observed may be related to the precociality of Sigmodon. We suggest that Waddington's diagrammatic presentation of the “epigenetic landscape” may be misleading in quantitative studies of developmental regulation.     

Skeletal ossification and sequence heterochrony in xenarthran evolution

Previous analyses of how mammals vary in their ossification sequences have focused on monotremes, marsupials, and boreoeutherian placentals. Here, we focus on the sequence of cranial and postcranial ossification events during growth in the xenarthran skull and skeleton, including armadillos, anteaters, and sloths. We use two different methods to quantify sequence heterochrony: sequence analysis of variance (ANOVA) and event‐paring/Parsimov. Our results indicate that Parsimov is conservative and does not detect clear heterochronic shifts between xenarthran and boreoeutherian placentals. Sequence‐ANOVA performs better, but both methods exhibit sensitivity to the artifactual accumulation of ties. By controlling for ties and taking into account results that the methods have in common, our analysis suggests that xenarthrans significantly differ from other placentals by a late ossification of the sternum and an early ossification of the phalanges and pubis. We interpret these differences as showing that heterochrony plays a role in the skeletal development of xenarthrans, a change from previous studies that have emphasized the developmental homogeneity of the skeleton across placental mammals.     

Butterfly wing pattern mutants: developmental heterochrony and co-ordinately regulated phenotypes

Butterfly wings are colored late in development, when pigments are synthesized in specialized wing scale cells in a fixed developmental succession. In this succession, colored pigments are deposited first and the remaining areas are later melanized black or brown. Here we studied the developmental changes underlying two wing pattern mutants, firstly melanic mutants of the swallowtail Papilio glaucus, in which the yellow background is turned black, and secondly a Spotty mutant of the satyrid Bicyclus anynana, which carries two additional eyespots. Despite the very different pattern changes in these two mutants, they are both associated with changes in rates of scale development and correspondingly, the final color pattern. In the melanic swallowtail, background scales originally destined to become yellow (normally developing early and synthesizing papiliochrome) show delayed development, fail to make papiliochrome, and subsequently melanize at the same time as scales in the wild-type black pattern. In the B. anynana eyespot, scale maturation begins with the central white focus, then progresses to the surrounding gold ring and later finishes with melanization of the black center. Mutants showing additional eyespots display accelerated rates of scale development (corresponding to new eyespots) in wing cells not normally occupied by eyespots. Thus by either delaying or accelerating rates of scale development, the final color, or position, of a wing pattern element can be changed. We propose that this heterochrony of scale development is a basic mechanism of color pattern formation on which developmental mutants act to change lepidopteran color patterns. Received: 20 April 2000 / Accepted: 19 July 2000     

Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill

The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as Triceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.