Convergent occurrence of the developmental hourglass in plant and animal embryogenesis?

Background The remarkable similarity of animal embryos at particular stages of development led to the proposal of a developmental hourglass. In this model, early events in development are less conserved across species but lead to a highly conserved ‘phylotypic period’. Beyond this stage, the model suggests that development once again becomes less conserved, leading to the diversity of forms. Recent comparative studies of gene expression in animal groups have provided strong support for the hourglass model. How and why might such an hourglass pattern be generated? More importantly, how might early acting events in development evolve while still maintaining a later conserved stage?Scope The discovery that an hourglass pattern may also exist in the embryogenesis of plants provides comparative data that may help us explain this phenomenon. Whether the developmental hourglass occurs in plants, and what this means for our understanding of embryogenesis in plants and animals is discussed. Models by which conserved early-acting genes might change their functional role in the evolution of gene networks, how networks buffer these changes, and how that might constrain, or confer diversity, of the body plan are also discused.Conclusions Evidence of a morphological and molecular hourglass in plant and animal embryogenesis suggests convergent evolution. This convergence is likely due to developmental constraints imposed upon embryogenesis by the need to produce a viable embryo with an established body plan, controlled by the architecture of the underlying gene regulatory networks. As the body plan is largely laid down during the middle phases of embryo development in plants and animals, then it is perhaps not surprising this stage represents the narrow waist of the hourglass where the gene regulatory networks are the oldest and most robust and integrated, limiting species diversity and constraining morphological space.     

How can a character be developmentally constrained despite variation in developmental pathways?

A fundamental riddle of evolutionary developmental biology is the conservation of adult morphological patterns (Hall, 1992). Conservative patterns are either called body plans if they concern overall body design, or homologues if they concern parts of the body (Riedl, 1978; Roth, 1982; Sattler, 1984; Van Valen, 1982; Wagner, 1989a, 1989b). An adult pattern is considered conservative if it remains unchanged in spite of changes in function, as indicated by the original definition of homology by Owen, as a similarity of organs regardless of form and function (Owen, 1848). Conservation of anatomical features despite different adaptive pressures is naturally explained by developmental constraints (Wagner, 1986). However, this approach to explain the biological basis of homology is plagued by the fact that developmental pathways are often more variable than the characters that they produce (see Tab. 1) (Hall, 1992; Roth, 1988, 1991; Spemann, 1915; Wagner, 1989b). This is also true for any other application of the concept of developmental constraints. The widely held opinion that early stages of development are conservative because any early perturbation is likely to interfere with later development, is far from absolute, since a vast amount of data in comparative developmental biology speaks to developmental variation (see e.g. the examples in Tab. 1). The question then is, how can developmental constraints on adult variation be reconciled with the fact of developmental variation?     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.     

Vicariance, climate change, anatomy and phylogeny of Restionaceae

Cutler suggested almost 30 years ago that there was convergent evolution between African and Australian Restionaceae in the distinctive culm anatomical features of Restionaceae. This was based on his interpretation of the homologies of the anatomical features, and these are here tested against a 'supertrec' phylogeny, based on three separate phvlogenies. The first is based on morphology and includes all genera; the other two are based on molecular sequences from the chloroplast genome-, one covers the African genera, and the other tin-Australian genera. This analysis corroborates Cutler's interpretation of convergent evolution between African and Australian Restionaceae. However, it indicates that for the Australian genera, the evolutionary pathway of the culm anatomy is much more complex than originally thought. In the most likely scenario, the ancestral Restionaceae have protective cells derived from the chlorenchyma. These persist in African Restionaceae, but are soon lost in Australian Restionaceae. Pillar cells and sclerenchyma ribs evolve early in the diversification of Australian Restionaceae, but are secondarily lost numerous times. In some of the reduction cases, the result is a very simple culm anatomy, which Cutler had interpreted as a primitively simple culm type, while in other cases it appears as if the functions of the ribs and pillars may have been taken over by a new structure, protective cells developed from epidermal, rather than chlorenchyma, cells. Cutler suggested that this convergent evolution might have been in response to Tertiary climatic deterioration, but this study finds no strong corroborating evidence for this.     

Altered retinoic acid signalling underpins dentition evolution

Small variations in signalling pathways have been linked to phenotypic diversity and speciation. In vertebrates, teeth represent a reservoir of adaptive morphological structures that are prone to evolutionary change. Cyprinid fish display an impressive diversity in tooth number, but the signals that generate such diversity are unknown. Here, we show that retinoic acid (RA) availability influences tooth number size in Cyprinids. Heterozygous adult zebrafish heterozygous for the cyp26b1 mutant that encodes an enzyme able to degrade RA possess an extra tooth in the ventral row. Expression analysis of pharyngeal mesenchyme markers such as dlx2a and lhx6 shows lateral, anterior and dorsal expansion of these markers in RA-treated embryos, whereas the expression of the dental epithelium markers dlx2b and dlx3b is unchanged. Our analysis suggests that changes in RA signalling play an important role in the diversification of teeth in Cyprinids. Our work illustrates that through subtle changes in the expression of rate-limiting enzymes, the RA pathway is an active player of tooth evolution in fish.     

Two developmentally temporal quantitative trait loci underlie convergent evolution of increased branchial bone length in sticklebacks

In convergent evolution, similar phenotypes evolve repeatedly in independent populations, often reflecting adaptation to similar environments. Understanding whether convergent evolution proceeds via similar or different genetic and developmental mechanisms offers insight towards the repeatability and predictability of evolution. Oceanic populations of threespine stickleback fish, Gasterosteus aculeatus, have repeatedly colonized countless freshwater lakes and streams, where new diets lead to morphological adaptations related to feeding. Here, we show that heritable increases in branchial bone length have convergently evolved in two independently derived freshwater stickleback populations. In both populations, an increased bone growth rate in juveniles underlies the convergent adult phenotype, and one population also has a longer cartilage template. Using F₂ crosses from these two freshwater populations, we show that two quantitative trait loci (QTL) control branchial bone length at distinct points in development. In both populations, a QTL on chromosome 21 controls bone length throughout juvenile development, and a QTL on chromosome 4 controls bone length only in adults. In addition to these similar developmental profiles, these QTL show similar chromosomal locations in both populations. Our results suggest that sticklebacks have convergently evolved longer branchial bones using similar genetic and developmental programmes in two independently derived populations.     

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen.     

Evolution of terrestrial birds in three continents: biogeography and parallel radiations

Aim To reconstruct the biogeographical history of a large clade of mainly terrestrially adapted birds (coraciiform and piciform birds, owls, diurnal raptors, New World vultures, trogons, mousebirds, cuckoo‐rollers, seriemas, parrots and passerines) to test the hypothesis of its Gondwanan origin. Location Global. Methods The phylogenetic tree used in the analysis was a family‐level tree estimated from previously published nuclear DNA sequence data. Each family for which a thorough and taxonomically well‐sampled phylogenetic analysis exists was subject to an initial dispersal–vicariance analysis in order to reconstruct ancestral areas for its two most basal lineages. Both basal lineages were then used to represent the family in the subsequent reconstruction of ancestral distributions for the entire radiation. Results The analysis showed that three reciprocally monophyletic groups of terrestrial birds have diversified in the Gondwanan land areas of Australia, South America and Africa, respectively. Although each of these three groups may also have originally included other groups, the only survivors today from the Australian radiation are the passerines and parrots, while the falcons and seriemas have survived from the South American radiation. The group of survivors from the African radiation is considerably more taxonomically diverse and includes all coraciiform and piciform birds, owls, diurnal raptors (except falcons), New World vultures, trogons, mousebirds and cuckoo‐rollers. Main conclusions The outlined evolutionary scenario with three geographically isolated clades of terrestrial birds is consistent with the available estimates of Late Cretaceous to early Palaeogene dates for these radiations. The diversifications and ecological adaptations within each of the three groups most likely took place in isolation on the different continents. Many cases of convergently evolved adaptations may be revealed through the increased understanding of the phylogenetic relationships of terrestrial birds.     

Testing models of dental development in the earliest bony vertebrates, Andreolepis and Lophosteus

Theories on the development and evolution of teeth have long been biased by the fallacy that chondrichthyans reflect the ancestral condition for jawed vertebrates. However, correctly resolving the nature of the primitive vertebrate dentition is challenged by a dearth of evidence on dental development in primitive osteichthyans. Jaw elements from the Silurian-Devonian stem-osteichthyans Lophosteus and Andreolepis have been described to bear a dentition arranged in longitudinal rows and vertical files, reminiscent of a pattern of successional development. We tested this inference, using synchrotron radiation X-ray tomographic microscopy (SRXTM) to reveal the pattern of skeletal development preserved in the sclerochronology of the mineralized tissues. The tooth-like tubercles represent focal elaborations of dentine within otherwise continuous sheets of the dermal skeleton, present in at least three stacked generations. Thus, the tubercles are not discrete modular teeth and their arrangement into rows and files is a feature of the dermal ornamentation that does not reflect a polarity of development or linear succession. These fossil remains have no bearing on the nature of the dentition in osteichthyans and, indeed, our results raise questions concerning the homologies of these bones and the phylogenetic classification of Andreolepis and Lophosteus.