No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Molecular Heterochronies and Heterotopies in Early Echinoid Development
Abstract
By comparing the spatial and temporal distribution of three proteins during early development in seven echinoid species, we demonstrate that both heterochronies and heterotopies in gene-product expression have accompanied the radiation of post-Paleozoic echinoids. All three proteins examined showed significant alterations in time of expression, site of expression, or both. These molecular heterochronies and heterotopies indicate that early development is not necessarily as evolutionarily conservative as morphology of embryos alone would suggest. Evolutionary alterations in early development may be more common than is generally assumed.
... Comparative studies of ontogeny provide unique windows into evolutionary mechanisms, permitting recognition of constraints on morphological evolution and of the proximal processes responsible for evolutionary change, as well as helping to elucidate phylogenetic patterns (seeWagner et al. 2000). Not surprisingly, several attempts have been made to recognize the modes by which ontogeny can be modified (e.g.,Zimmermann 1959;Takhtajan 1972;Gould 1977Gould , 2000Alberch et al. 1979;McNamara 1986a;Atchley 1987;Regier and Vlahos 1988;Raff and Wray 1989;Wray and McClay 1989;McKinney and McNamara 1991;Sattler 1992;Alberch and Blanco 1996;Raff 1996;Zelditch and Fink 1996;Reilly et al. 1997;Rice 1997;Klingenberg 1998;Lovejoy et al. 1999;Arthur 2000;Li and Johnston 2000;Sundberg 2000;Smith 2001). In this paper we present a novel consideration of modes of evolution because those previously proposed offer incomplete and sometimes confusing characterizations of ontogenetic modifications. ...
... Various non-heterochronic modes of developmental reprogramming have been proposed (see below), but each is potentially subject to the same problems as the concept of heterochrony. The problems plaguing heterochrony are in most immediate danger of being repeated by the concept of heterotopy (a change in the topology of development; Haeckel 1875;Gould 1977;Wray and McClay 1989;Zelditch and Fink 1996;Li and Johnston 2000). Some workers have considered heterotopy as a modification to spatial aspects of morphological development (e.g.,Zelditch and Fink 1996;Webster et al. 2001). ...
Consideration of the ways in which ontogenetic development may be modified to give morphological novelty provides a conceptual framework that can greatly assist in formulating and testing hypotheses of patterns and constraints in evolution. Previous attempts to identify distinct modes of ontogenetic modification have been inconsistent or ambiguous in definition, and incomprehensive in description of interspecific morphological differences. This has resulted in a situation whereby almost all morphological evolution is attributed to heterochrony, and the remainder is commonly either assigned to vague or potentially overly inclusive alternative classes, or overlooked altogether. The present paper recognizes six distinct modes of ontogenetic change, each a unique modification to morphological development: (1) rate modification, (2) timing modification, (3) heterotopy, (4) heterotypy, (5) heterometry, and (6) allometric repatterning. Heterochrony, modeled in terms of shape/time/size ontogenetic parameters, relates to parallelism between ontogenetic and phylogenetic shape change and results from a rate or timing modification to the ancestral trajectory of ontogenetic shape change. Loss of a particular morphological feature may be described in terms of timing modification (extreme postdisplacement) or heterometry, depending on the temporal development of the feature in the ancestor. Testing hypotheses of the operation of each mode entails examining the morphological development of the ancestor and descendant by using trajectory-based studies of ontogenetically dynamic features and non-trajectory-based studies of ontogenetically static features. The modes identified here unite cases based on commonalities of observed modification to the process of morphological development at the structural scale. They may be heterogeneous or partially overlapping with regard to changes to genetic and cellular processes guiding development, which therefore require separate treatment and terminology. Consideration of the modes outlined here will provide a balanced framework within which questions of evolutionary change and constraint within phylogenetic lineages can be addressed more meaningfully.
... The sister group of the euechinoids, the cidaroids or 'pencil urchins,' lack this feature. Their embryonic skeleton is formed instead by mesenchyme cells delaminating only at gastrulation (Wray and McClay, 1989). In euechinoids such as Strongylocentrotus, the secondary mesenchyme that delaminates at gastrulation in fact also retains skeletogenic capacity, which is normally repressed, but which can be elicited by depletion of the primary skeletogenic cells descendant from the micromeres (reviewed by Ettensohn, 1992). ...
... It would be interesting to know how recent this developmental mechanism is in origin. In Eucidaris tribuloides, a cidaroid sea urchin, the skeletogenic lineage founder cells are also segregated precociously, but micromeres per se form only irregularly (Wray and McClay, 1989): do they play the same inductive role? All modern sea urchins descend from a single cidaroidlike genus that survived the Permian extinction 230 mya (Smith, 1984) and the mode of veg2 specification in a living cidaroid would thus be revealing. ...
An early set of blastomere specifications occurs during cleavage in the sea urchin embryo, the result of both conditional and autonomous processes, as proposed in the model for this embryo set forth in 1989. Recent experimental results have greatly illuminated the mechanisms of specification in some early embryonic territories, though others remain obscure. We review the progressive process of specification within given lineage elements, and with reference to the early axial organization of the embryo. Evidence for the conditional specification of the veg2 lineage subelement of the endoderm and other potential interblastomere signaling interactions in the cleavage-stage embryo are summarized. Definitive boundaries between mesoderm and endoderm territories of the vegetal plate, and between endoderm and overlying ectoderm, are not established until later in development. These processes have been clarified by numerous observations on spatial expression of various genes, and by elegant lineage labeling studies. The early specification events depend on regional mobilization of maternal regulatory factors resulting at once in the zygotic expression of genes encoding transcription factors, as well as downstream genes encoding proteins characteristic of the cell types that will much later arise from the progeny of the specified blastomeres. This embryo displays a maximal form of indirect development. The gene regulatory network underlying the embryonic development reflects the relative simplicity of the completed larva and of the processes required for its formation. The requirements for postembryonic adult body plan formation in the larval rudiment include engagement of a new level of genetic regulatory apparatus, exemplified by the Hox gene complex.
... And as might be expected, some heterochronies likely arose in each of the three species. Gildor and Ben-Tabou de Leon later showed that heterochronies are present in a comparison between sea stars and Pl separated by about 500 million years since a common ancestor [55], and we showed evidence of heterochronies in a comparison of Lv with a cidaroid species separated by about 200 million years [56]. In each of those cases other evidence also shows a partial remodeling of the dGRNs [57,58]. ...
The developmental gene regulatory networks (dGRNs) of two sea urchin species, Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp), have remained remarkably similar despite about 50 million years since a common ancestor. Hundreds of parallel experimental perturbations of transcription factors with similar outcomes support this conclusion. A recent scRNA-seq analysis suggested that the earliest expression of several genes within the dGRNs differs between Lv and Sp. Here, we present a careful reanalysis of the dGRNs in these two species, paying close attention to timing of first expression. We find that initial expression of genes critical for cell fate specification occurs during several compressed time periods in both species. Previously unrecognized feedback circuits are inferred from the temporally corrected dGRNs. Although many of these feedbacks differ in location within the respective GRNs, the overall number is similar between species. We identify several prominent differences in timing of first expression for key developmental regulatory genes; comparison with a third species indicates that these heterochronies likely originated in an unbiased manner with respect to embryonic cell lineage and evolutionary branch. Together, these results suggest that interactions can evolve even within highly conserved dGRNs and that feedback circuits may buffer the effects of heterochronies in the expression of key regulatory genes.
Supplementary Information
The online version contains supplementary material available at 10.1186/s13227-023-00214-y.
... In the ancestral condition, msp130 is expressed around the time that the precursors of the skeletogenic cells begin to undergo ingression, an epithelial-to-mesenchymal transition (Anstrom et al., 1987). Although there are some minor differences in timing of expression among species with planktotrophic larvae (Wray & McClay, 1989), expression is delayed by several hours in H. erythrogramma (Parks et al., 1988). Several other components of the "biomineralization toolkit" of sea urchins (Karakostis et al., 2016) also show and delay or reduction in overall expression in H. erythrogramma (Israel et al., 2016). ...
As analyses of developmental mechanisms extend to ever more species, it becomes important to understand not just what is conserved or altered during evolution, but why. Closely related species that exhibit extreme phenotypic divergence can be uniquely informative in this regard. A case in point is the sea urchin genus Heliocidaris, which contains species that recently evolved a life history involving nonfeeding larvae following nearly half a billion years of prior evolution with feeding larvae. The resulting shift in selective regimes produced rapid and surprisingly extensive changes in developmental mechanisms that are otherwise highly conserved among echinoderm species. The magnitude and extent of these changes challenges the notion that conservation of early development in echinoderms is largely due to internal constraints that prohibit modification and instead suggests that natural selection actively maintains stability of inherently malleable trait developmental mechanisms over immense time periods. Knowing how and why natural selection changed during the evolution of nonfeeding larvae can also reveal why developmental mechanisms do and do not change in particular ways.
... Wray et al. (2003) distinguished the following classes of evolutionary change in gene expression: -changes in the spatial extent of gene expression. (e.g., Schiff et al. 1992;Brunetti et al. 2001;Scemama et al. 2002) -changes in the timing of gene expression (transcriptional heterochrony), as documented for many taxa (e.g., Wray & McClay 1989;Kim et al. 2000;Skaer et al. 2002). For example, the bristle pattern on the notum of Diptera is regulated by the expression of the gene scute. ...
Evolutionary developmental biology (evo-devo) suggests a distinction between modular and systemic variation. In the case of modular change, the conservation of the overall structure helps recognizing affinities, while a single, fast evolving module is likely to produce a bonanza for the taxonomist, while systemic changes produce strongly deviating morphologies that cause problems in tracing homologies. Similarly, changes affecting the whole life cycle are more challenging than those limited to one stage. Developmental modularity is a precondition for heterochrony. Analyzing a matrix of morphological data for paedomorphic taxa requires special care. It is, however, possible to extract phylogenetic signal from heterochronic patterns. The taxonomist should pay attention to the intricacies of the genotype-->. phenotype map. When using genetic data to infer phylogeny, a comparison of gene sequences is just a first step. To bridge the gap between genes and morphology we should consider the spatial and temporal patterns of gene expression, and their regulation. Minor genetic change can have major phenotypic effects, sometimes suggesting saltational evolution. Evo-devo is also relevant in respect to speciation: changes in developmental schedules are often implicated in the divergence between sympatric morphs, and a developmental modulation of 'temporal phenotypes' appears to be responsible for many cases of speciation.
... The protein mspl3O provides a specific probe for these cells. This protein is produced only by primary mesen chyme cells in euechinoid embryos (Anstrom et a!., 1987;Wray and McClay, 1989) and by skeletogenic cells in adults (Parks et a!., 1988). In planktotrophic larvae of the cidaroid Eucidaris tribu!oides, there are 16 spicule forming cells, homologous to euechinoid primary mes enchyme cells, that express mspl3O (Wray and McClay, 1988). ...
Development in the Australian sea urchin Phyllacanthus parvispinus (Echinoidea: Cidaroidea) is of interest because it has a highly modified, lecithotrophic larva, and because it belongs to an echinoid group whose development has been little studied. This study documents early development and metamorphosis in P. parvispinus and considers the evolution of features unusual in echinoid ontogeny. Some features, such as lack of a vestibule, occur in other cidaroids, and are likely a product of ancestry. Other unusual features, such as larger gametes, an equal fourth cleavage, a wrinkled blastula, and accelerated development of the adult rudiment, are characteristic of other direct developing echinoids, and are probably functional modifications for altered developmental mode. Since the Cidaroidea form the sister group to the more derived Euechinoidea, cidaroid development is critical in assessing the phylogeny of ontogeny among echinoids. The distribution of developmental features among extant echinoids suggests that the extinct ancestor of cidaroids and euechinoids had planktotrophic larvae that lacked a vestibule during formation of the juvenile rudiment.
... Our results are therefore evidence for heteroposy in the evolution of the Ardeidae: we report evolutionary transformations in tarsometatarsal growth rates and morphology which are the outcome of changes in the amount of proliferating cells at growth plates. The concept of heteroposy should be added to Haeckel's (1866) concepts of heterochrony (evolutionary changes of developmental timing and rates, Klingenberg, 1998) and heterotopy (evolutionary changes in the location of a developmental event, Wray & McClay, 1989), in order to complete our understanding of this kind of evolutionary phenomena. ...
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.
... These observations support the view that the invention of the micromere-PMC lineage was associated with a heterochronic shift in the deployment of an ancestral GRN that was operative in the late-ingressing skeletogenic mesenchyme of ancestral echinoids. This mode of skeletogenesis is still seen in modern cidaroid urchins, which closely resemble the ancestral stock that gave rise to all extant sea urchins (Wray and McClay, 1989). It seems likely that one vestige of this heterochronic shift that has been retained in modern euechinoid sea urchins is the biphasic temporal expression (i.e. ...
A central challenge of developmental and evolutionary biology is to understand how anatomy is encoded in the genome. Elucidating the genetic mechanisms that control the development of specific anatomical features will require the analysis of model morphogenetic processes and an integration of biological information at genomic, cellular and tissue levels. The formation of the endoskeleton of the sea urchin embryo is a powerful experimental system for developing such an integrated view of the genomic regulatory control of morphogenesis. The dynamic cellular behaviors that underlie skeletogenesis are well understood and a complex transcriptional gene regulatory network (GRN) that underlies the specification of embryonic skeletogenic cells (primary mesenchyme cells, PMCs) has recently been elucidated. Here, we link the PMC specification GRN to genes that directly control skeletal morphogenesis. We identify new gene products that play a proximate role in skeletal morphogenesis and uncover transcriptional regulatory inputs into many of these genes. Our work extends the importance of the PMC GRN as a model developmental GRN and establishes a unique picture of the genomic regulatory control of a major morphogenetic process. Furthermore, because echinoderms exhibit diverse programs of skeletal development, the newly expanded sea urchin skeletogenic GRN will provide a foundation for comparative studies that explore the relationship between GRN evolution and morphological evolution.
... However, Raff (15) has pointed out that heterochrony can be found in earlier as well as in later stages of development. Indeed, changes in developmental timing in the early stages of ontogeny has been described in many studies (6,(36)(37)(38)(39). Furthermore, Richardson et al. (40) argue that previous notions of phylotypic stages are based on an incomplete analysis of comparative data, and they suggest that there are no particularly conserved stages of development. ...
Heterochrony, the relative change of developmental timing, is one of the major modes of macroevolutionary change; it identifies temporally disassociated units of developmental evolution. Here, we report the results of a fine-scale temporal study for the expression of the developmental gene hairy and morphological development in three species of Drosophila, D. melanogaster, D. simulans, and D. pseudoobscura. The results suggest that between and among closely related species, temporal displacement of ontogenetic trajectory is detected even at the earliest stage of development. Overall, D. simulans shows the earliest expression, followed by D. melanogaster, and then by D. pseudoobscura. Setting D. melanogaster as the standard, we find the approximate time to full expression is accelerated by 13 min, 48 s in D. simulans and retarded by 24 min in D. pseudoobscura. Morphologically, again with D. melanogaster setting the standard, initiation of cellularization is faster in D. simulans by 15 min, 42 s; and initiation of morphogenesis is faster in D. simulans by 18 min, 7 s. These results seem to be consistent with the finding that the approximate time to full expression of hairy is accelerated by 13 min, 48 s in D. simulans. On the other hand, the same morphological events are delayed by 5 min, 32 s, and by 11 min, 32 s, respectively, in D. pseudoobscura. These delays are small, compared with the 24-min delay in full expression. The timing changes, in total, seem consistent with continuous phyletic evolution of temporal trajectories. Finally, we speculate that epigenetic interactions of hairy expression timing and cell-cycle timing may have led to morphological differences in the terminal system of the larvae.
... Based on our data, we suggest that heterochrony alone is not an adequate explanation for the divergence of phenotypes in populations undergoing rapid ecological divergence. It appears that evolutionary divergence occurs both for rates and for trajectories of shape ontogeny among charr ecomorphs (Wray & McClay, 1989; Zelditch & Fink, 1996; Zelditch et al., 2000). ...
Phenotypic plasticity is a developmental process that plays a role as a source of variation for evolution. Models of adaptive divergence make the prediction that increasing ecological specialization should be associated with lower levels of plasticity. We tested for differences in the magnitude, rate and trajectory of morphological plasticity in two lake populations of Arctic charr (Salvelinus alpinus) that exhibited variation in the degree of resource polymorphism. We reared offspring on diet treatments that mimicked benthic and pelagic prey. Offspring from the more divergent population had lower levels of morphological plasticity. Allometry influenced the rate of shape change over ontogeny, with differences in rate among ecomorphs being minimal when allometric variation was removed. However, plasticity in the spatial trajectory of development was extensive across ecomorphs, both with and without the inclusion of allometric variation, suggesting that different aspects of shape development can evolve independently.
... Direct development is the opposite, the loss of larval or juvenile traits, resulting in the immediate appearance of the adult form of a trait early in development (Gilbert 1997). Examples of heterochrony abound in the literature, and include the evolution of morphological (Raff 1987) and behavioral traits (Garie`py et al. 2001), as well as gene expression (Wray and McClay 1989). Heterochrony is postulated to play an important role in phenotypic evolution, as it can generate new combinations of adult and larval phenotypes for selection to act upon (Gould 1977;McKinney and McNamara 1991;West-Eberhard 2003). ...
SUMMARY Lake Malawi (LM) cichlids have undergone heterochronic shifts in the expression of their cone opsin genes, the genes responsible for color vision. These shifts have generated species with short-, middle-, and long-wavelength-sensitive cone photoreceptors and visual systems. However, it is unclear when during the evolution of African cichlids these shifts occurred, or whether they could account for similar short- and middle-wavelength-sensitive profiles among unrelated cichlids in Lake Tanganyika (LT). To address these questions, we surveyed opsin expression in developing fry of two African cichlids, Astatotilapia burtoni from LT and Melanochromis auratus from LM. We found that A. burtoni expresses a series of three different single-cone opsins over the course of development, while M. auratus exhibits variation in the expression of only two. Neither A. burtoni nor M. auratus exhibits much variation in the expression of its double-cone opsins. These patterns reveal that A. burtoni exhibits progressive development in the sensitivity of its single-cone photoreceptors, but direct development in the sensitivity of its double-cone photoreceptors. M. auratus exhibits neotenic development in the sensitivity of both photoreceptor sets. Given the intermediate phylogenetic placement of A. burtoni between cichlids from LT and LM, our results suggest that the ancestor of LM's cichlids exhibited a progressive developmental pattern of opsin expression. These results indicate that the heterochronic shifts which produced the short- and middle-wavelength-sensitive profiles of LM's cichlids occurred recently, and suggest that the presence of similar profiles among LT's cichlids are due to parallel heterochronic shifts.
... Detailed comparisons between related species reveal at what level developmental mechanisms and processes are evolving: for example, in the case of sturgeon and Xenopus gastrulation the morphogenetic mechanisms that produce extension are highly conserved, but the pattern in which they are expressed has changed along with the geometry of the embryos. In other systems, evolutionarily critical changes have evolved during the earliest stages of development (Wray and Raff, 1989;Raff, 1992). ...
SYNOPSIS. Comparative embryological studies of frogs and fish provide valuable information about the mechanisms and evolution of vertebrate development. First, by mapping developmental data from a range of species onto a cladogram, one can distinguish general features of a ground plan from variation within it. Two studies illustrate this: comparison of gastrulation mechanisms in sturgeon and Xenopus , and morphogenesis of the dorsal mesoderm in five species of anurans. Second, phylogenetic analysis of developmental data makes it possible to identify radical departures from the ground plan among related groups. Teleost gastrulation is a highly derived process that appears to have little in common with the ancestral version. However, teleost gastrulation may have evolved as a result of two specific developmental changes: loss of bottle cells in the surface layer, and changes in the yolk. The phylogenetic distribution of developmental characters forms the basis for mechanistic hypotheses about the origins of major evolutionary changes in development
... Changes in the timing and order of internal organ system morphogenesis, in stage of founder cell specification , and in timing of expression of lineage-specific marker genes (Parks et al. 1988; Raff et al. 1990; Wray and Raff, 1990) are among the differences that distinguish direct development in sea urchins from typical indirect development. Indeed heterochronic (and other) changes in lineage specific gene expression can be observed even in comparing various indirectly developing sea urchin species (Wray and McClay, 1989). For the most part, species belonging to typically Type 1 phyla, which display direct development, nonetheless retain a Type 1 form of embryonic process, by the external criteria of Tablel. ...
The basic characteristics of embryonic process throughout Metazoa are considered with focus on those aspects that provide insight into how cell specification occurs in the initial stages of development. There appear to be three major types of embryogenesis: Type 1, a general form characteristic of most invertebrate taxa of today, in which lineage plays an important role in the spatial organization of the early embryo, and cell specification occurs in situ, by both autonomous and conditional mechanisms; Type 2, the vertebrate form of embryogenesis, which proceeds by mechanisms that are essentially independent of cell lineage, in which diffusible morphogens and extensive early cell migration are particularly important; Type 3, the form exemplified by long germ band insects in which several different regulatory mechanisms are used to generate precise patterns of nuclear gene expression prior to cellularization. Evolutionary implications of the phylogenetic distribution of these types of embryogenesis are considered. Regionally expressed homeodomain regulators are utilized in all three types of embryo, in similar ways in later and postembryonic development, but in different ways in early embryonic development. A specific downstream molecular function for this class of regulator is proposed, based on evidence obtained in vertebrate systems. This provides a route by which to approach the comparative regulatory strategies underlying the three major types of embryogenesis.
... The small changes in the onset of msp130 expression (Fig. 3, white bars) are not associated with life history differences or adult morphology, and must be explained in another way. In most species, msp130 protein appears before skeletogenesis actually begins (Wray and McClay, 1989). Activating msp130 transcription slightly before it is required may not be detrimental . ...
We analyzed a comparative data base of gene expression, cell fate specification, and morphogenetic movements from several echinoderms to determine why developmental processes do and do not evolve. Mapping this comparative data onto explicit phylogenetic frameworks revealed three distinct evolutionary patterns. First, some evolutionary differences in development correlate well with larval ecology but not with adult morphology. These associations are probably not coincidental because similar developmental changes accompany similar ecological transformations on separate occasions. This suggests that larval ecology has been a potent influence on the evolution of early development in echinoderms. Second, a few changes in early development correlate with transformations in adult morphology. Because most such changes have occurred only once, however, it is difficult to distinguish chance associations from causal relationships. And third, some changes in development have no apparent phenotypic consequences and do not correlate with obvious features of either life history or morphology. This suggests that some evolutionary changes in development may evolve in a neutral or nearly neutral mode. Importantly, these hypotheses make specific predictions that can be tested with further comparative data and by experimental manipulations. Together, our phylogenetic analyses of comparative data suggest that at least three distinct evolutionary mechanisms have shaped early development in echinoderms.
... The HeARS gene in H. erythrogramma may represent a cooption of a structural gene whose function ancestrally was in development of the larval body into the accelerated process of rudiment development, and is therefore a heterotopy which accompanied the evolution of direct development. Such evolutionary heterotopies do not necessarily yield morphological novelty, as they have been shown to exist in different species of pluteus-forming sea urchins (Wray and McClay 1989). However, they indicate an underlying genomic flexibility that provides raw material for the evolution of development (Raff 1996). ...
The Australian sea urchin Heliocidaris erythro-gramma utilizes a derived direct developmental mode that evolved 8-12 million years ago. From a differential screen we have isolated a small set of cDNAs corresponding to genes more greatly expressed in embryos of H. erythrogramma than in those of its indirect-developing nearest relative, H. tuberculata. The method was biased towards abundant transcripts and did not allow detection of modifications of usage of highly conserved gene family members. Three differentially expressed abundant transcripts were found that potentially encode secreted proteins. Two of these, the arylsulfatase HeARS and the putative lectin HeEL-1, were identifiable as homologues of known proteins. Another gene, HeET-1, may be exclusively expressed in the H. erythrogramma embryo. In situ hybridization experiments demonstrate that all three transcripts are localized to the ectoderm. Two of them, HeET-1 and HeEL-1, are transcribed in an identical domain comprising the larval ectoderm. This region of gene expression has acquired a novel columnar cytology during the evolution of the H. erythrogramma embryo. The third sequence, HeARS, encodes an arylsulfatase homologue. Its expression is uniform in the gastrula, but as the rudiment develops it accumulates to the greatest extent in the invaginating vestibular ectoderm. Through comparisons with indirect-developing species, we show that this concentration of arylsulfatase mRNA in the rudiment is a novel feature of H. erythrogramma development. These data suggest that H. erythrogramma has a unique arrangement of ectodermal gene expression territories. We propose that these reflect larval adaptations that have occurred in the lineage leading to H. erythrogramma, and enabled the evolution of direct development.
New developmental programs can evolve through adaptive changes to gene expression. The annelid S. benedicti has a developmental dimorphism, which provides a unique intraspecific framework for understanding the earliest genetic changes that take place during developmental divergence. Using comparative RNAseq through ontogeny, we find that only a small proportion of genes are differentially expressed at any time, despite major differences in larval development and life-history. These genes shift expression profiles across morphs by either turning off any expression in one morph or changing the timing or amount of gene expression. We directly connect the contributions of these mechanisms to differences in developmental processes. We examine F 1 offspring —using reciprocal crosses— to determine maternal mRNA inheritance and the regulatory architecture of gene expression. These results highlight the importance of both novel gene expression and heterochronic shifts in developmental evolution, as well as the trans -acting regulatory factors in initiating divergence.
Because development is epigenetic, diverse aspects of morphology are integrated during ontogeny. Using the method of thin-plate splines, and the decomposition of these splines by their principal warps, we examine the ontogeny of integrated features of skull growth of the cotton rat, Sigmodon fulviventer as observed in landmark locations in the ventral view. Postnatal growth of the skull in Sigmodon is not adequately described by the familiar contrast between relatively rapid facial elongation and slow, precocial growth of the cranial base. No developmental units corresponding to "facial skull" and "cranial base" emerge from analysis of geometric shape change. Rather, skull growth is both more integrated and more complex, exhibiting both skull-wide integration and locally individualized regions. Like skull shape, integration has an ontogeny; different regions of the skull can be partitioned into developmentally individualized parts in different ways at different ages. The effective count of individualized parts decreases substantially before weaning occurs, suggesting that the integration required by the functionally demanding activity of chewing gradually develops before the functional transition occurs. Our description of skull growth and integration does not depend upon arbitrary a priori choices about what to measure; rather, we base our decomposition of the whole into parts upon results of the data analysis. Our approach complicates the study of heterochrony, but, because it expresses the spatiotemporal organization of ontogeny, it enables the study of heterotopy.
Significance
Sea urchins (echinoids) consist of two subclasses, cidaroids and euechinoids. Research on gene regulatory networks (GRNs) in the early development of three euechinoids indicates that little appreciable change has occurred to their linkages since they diverged ∼90 million years ago (mya). I asked whether this conservation extends to all echinoids. I systematically analyzed the spatiotemporal expression and function of regulatory genes segregating euechinoid ectoderm and mesoderm in a cidaroid. I report marked divergence of GRN architecture in early embryonic specification of the oral–aboral axis in echinoids. Although I found evidence for diverged regulation of both mesodermal and ectodermal genes, comparative analyses indicated that, since these two clades diverged 268 mya, mesodermal GRNs have undergone significantly more alterations than ectodermal GRNs.
Ascidian development has been investigated by embryo-logists since the latter half of the nineteenth century (see Venuti and Jeffery, 1989 for a review) due to a number of desirable features. First, embryonic development is rapid. In most ascidians, gastrulation occurs only a few hours after fertilization, and embryogenesis is completed in less than a day. Second, ascidians are one of the simplest chordates: the tadpole larva contains only a few thousand cells and about 6 different types of tissue (Berrill, 1935). The ascidian genome is quite small for a chordate: only about 1.8 × 108 nucleotide pairs (Mirsky and Ris, 1951; Atkin and Ohno, 1967; Lambert and Laird, 1971). Third, ascidian embryos are highly mosaic: most cell fates are established according to a defined cell lineage (Chabry, 1887; Conklin, 1905a). Fourth, some ascidians have evolved alternative development modes, which are useful for examining developmental changes during evolution (Berrill, 1931; 1935). Finally, the eggs of the ascidian Styela contain colored ooplasms (Conklin, 1905b; Berrill, 1929). The most spectacular of these ooplasms is the yellow crescent or myoplasm, a unique cytoskeletal domain that segregates to the future posterior region of the zygote after fertilization (Conklin, 1905b; Jeffery, 1984). During cleavage, the myoplasm is distributed to 2 cells of the 2-,4-, and 8-cell embryo, 4 cells of the 16-cell embryo, 6 cells of the 32-cell embryo, 8 cells of the 64-cell embryo, and eventually enters the larval tail-muscle cells (Fig.l).
Does phylogeny build ontogenies, as Ernst Haeckel would have it, or do ontogenies make phylogeny, as Walter Garstang emphasized? Clearly, there is some relationship between ontogeny and phylogeny, since every change in phylogeny must result in changing ontogenies, while every change of ontogeny will cause a change in phylogeny. The problem is how to conceptualize this relationship to use it as a tool for phylogeny reconstruction, or to explore its significance for the evolution of complex and integrated organic systems. The problem simply is this: Do we require knowledge of a well-constrained phylogeny in order to explore the role of ontogeny in evolution? If so, how can we gain such knowledge of phylogeny? Or does the study of ontogeny provide us with a key to a well-constrained phylogeny? As this problem is a multilayered one, difficult to untangle, I propose to proceed as follows.
While a framework and terminology for heterochrony has been referenced widely in the literature and appears to be accepted by nearly all workers in the field we have found it to be a confusing and incomplete model that has led to varying degrees of misunderstanding about heterochrony among evolutionary biologists. Much of the confusion exists because the model is explicitly limited to phylogenetic patterns (interspecific comparisons), but has been used for intraspecific comparisons. Because heterochrony may underlie all morphological variation and possibly isthedevelopmental phenomenon producing all morphological change it is important that descriptions of heterochronic patterns and processes be clear and precise over all levels of analysis. To this end we discuss and clarify the previous model for heterochrony, reject some of the terminology and suggest alternatives, and then expand the model to include a new nomenclature for intraspecific heterochronic phenomena. Our modifications are essential to maintain the critical conceptual distinction between inter- vs. intraspecific heterochronic patterns and processes in evolutionary biology.
Since its inception in the early 1980s, evo-devo has evolved into a mature discipline. This is manifest in the naming of research groups, scientific journals and books, pr Of essional meetings and societies. Despite such formal attributes of a scientific discipline it is often unclear what constitutes its conceptual distinctiveness. Does evo-devo have its own set of specific questions and research methods? Does it solve biological problems that cannot be solved by other approaches? And does it represent a significant change in the theoretical understanding of development and evolution? That is, in which way do the goals, the empirical programs and the theories of evo-devo research differ from those of neighbouring disciplines such as developmental biology or evolutionary biology? The present chapter provides a concise overview of the current status of evo-devo as a discipline. This requires a short reflection on its history. CONCEPTUAL FOUNDATIONS The parallels between embryonic stages and the ‘scale of beings’ had already been contemplated in pre-Darwinian times, and the foundation of a scientific theory of evolution was significantly influenced by embryological arguments. Darwin called embryology ‘by far the strongest single class of facts in favour of a change of form’, and his first sketches of a phylogenetic tree seem to have been inspired by tree-like renderings of embryological differences between species (Richards 1992). Much of the early work in evolutionary biology focused on the uses of embryonic characters for taxonomical purposes. © Cambridge University Press 2008 and Cambridge University Press, 2009.
The purpose of this study is to describe and compare the organogenesis of adult leaves of different shapes in order to determine in what point during development differences in shape become apparent. The correlation between shape during development and that of mature leaves provides the basis for interpretation of the determination of shape differences
Evolution by natural selection requires variations that (a) exhibit fitness differences, and (b) are heritable. We use these criteria to examine what McDonald called a "great Darwinian paradox," namely, that there is little evidence for relevant variation at "those regulatory loci set deep with the control network" (1983, 92-3) of metazoan ontogenies. Currently, the absence of heritable variation in what Wimsatt calls the "deeply-entrenched" features of ontogeny has led many investigators to argue that profound temporal asymmetries exist in evolutionary history; in short, things were different in the pre-Cambrian. Yet it is unclear how ontogenetic architectures early in metazoan history could have differed fundamentally from present-day systems. We have commenced a survey of the literature of the principal model systems of evo-devo, as well as lesser-known systems, looking for evidence of heritable mutations in such features as cleavage patterns, axis specification, or modes of gastrulation. The continued absence of such evidence suggests that it may be time to re-examine basic assumptions.
▪ Abstract New robust phylogenies for echinoderms, based on congruent patterns derived from multiple data sets, provide a sound foundation for plotting the evolution of life-history strategies and comparing rates and patterns of larval and adult morphological change. This approach demonstrates that larval morphology has been evolving independently of adult morphology, that larval morphology displays more homoplasy than adult morphology, and that early developmental patterns are remarkably flexible. Larval morphology on its own can mislead phylogenetic analysis, not because of lateral gene transfer among distantly related taxa, but because of massive convergence in the form of nonfeeding larvae brought about by the loss of complex structures and the strong functional constraints on feeding larvae. The degree to which larval tissue is resorbed at metamorphosis is believed to be important in determining adult body plan. Although the correspondence is not precise, it does provide a model for understanding ske...
Recent advances in our understanding of developmental phenomena has come from highly interdisciplinary studies where molecular biology, ecology and evolution converge to elucidate fundamental mechanisms, how they change through time, and what function they actually have in the context of the niche of the organism. A recent study on butterfly eyespots(1) pinpoints the surprisingly simple regulatory cascade controlling such an apparently complex phenotype. The implications go beyond the elucidation of a fascinating developmental pathway, into the mechanisms and tempo of speciation and macroevolution.
Abstract How micro- and macroevolutionary evolutionary processes produce phenotypic change is without question one of the most intriguing and perplexing issues facing evolutionary biologists. We believe that roadblocks to progress lie A) in the underestimation of the role of the environment, and in particular, that of the interaction of genotypes with environmental factors, and B) in the continuing lack of incorporation of development into the evolutionary synthesis. We propose the integration of genetic, environmental and developmental perspectives on the evolution of the phenotype in the form of the concept of the developmental reaction norm (DRN) The DRN represents the set of multivariate ontogenies that can be produced by a single genotype when it is exposed to environmental variation. It encompasses: 1) the processes that alter the phenotype throughout the ontogenetic trajectory, 2) the recognition that different aspects of the phenotype are (and must be) correlated and 3) the ability of a genotype to produce phenotypes in different environments. This perspective necessitates the explicit study of character expression during development, the evaluation of associations between pairs or groups of characters (e.g., multivariate allometries), and the exploration of reaction norms and phenotypic plasticity. We explicitly extend the concept of the DRN to encompass adjustments made in response to changes in the internal environment as well. Thus, ‘typical’ developmental sequences (e.g., cell fate determination) and plastic responses are simply manifestations of different scales of ‘environmental’ effects along a continuum. We present: (1) a brief conceptual review of three fundamental aspects of the generation and evolution of phenotypes: the changes in the trajectories describing growth and differentiation (ontogeny), the multivariate relationships among characters (allometry), and the effect of the environment (plasticity); (2) a discussion of how these components are merged in the concept of the developmental reaction norm; and (3) a reaction norm perspective of major determinants of phenotypes: epigenesis, selection and constraint.
Although initial discussions and speculations about the role of acceleration and retardation in the relative timing of ontogenetic events associated with dental evolution, dental development, and heterodonty can be found in the literature as early as a century ago, morphogenetic processes and mechanisms remain elusive and formal heterochronic and mechanistic models employing mathematical principles, especially those that are testable, have only recently begun to appear. Even the seemingly simplest of developmental problems, such as primate canine tooth size variation in ontogeny and phylogeny, continue to be the subject of much controversy and debate. At least part of the problem, as well as its solution, may be found in the uniqueness of the process of amelogenesis during tooth formation and the dichotomy between inner enamel epithelium growth parameters and those dealing with ameloblast secretory functions, including duration and rate. Certain aspects of the life cycle of the inner enamel epithelium lend themselves to mathematical analysis and can be visualized graphically as a morphogenetic triangle, which illustrates the relationship between proliferation and differentiation during tooth crown formation. Components of the triangle model include the times of onset of proliferation (P), onset of differentiation (D), and crown completion (C), which provide the basis for calculations of rate of proliferation (RP) and rate of differentiation (Rd) during the attainment of final crown height measured at the dentinoenamel junction. Thus, tooth crown size is partially controlled by a “framework” established by the proliferating cells of the inner enamel epithelium, and partially by the variable thickness of enamel matrix produced by functional ameloblasts and laid down on the “framework” following their terminal differentiation. From a developmental point of view, it would seem appropriate to consider tooth size (inner enamel epithelium, morphogenetic triangle) and enamel thickness (secretory ameloblasts) as independent parameters of growth that contribute differentially to external crown dimensions. Morphogenetic triangle parameters that are actually related to real ontogenetic events during tooth formation facilitate heterochronic analysis and modelling and provide a theoretical basis for a broader understanding of basic mechanisms involved in certain troublesome size and shape problems in dental morphogenesis and evolution.
The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized. 2001 The Linnean Society of London ADDITIONAL KEY WORDS: development – craniofacial – mammal – marsupial.
While a framework and terminology for heterochrony has been referenced widely in the literature and appears to be accepted by nearly all workers in the field we have found it to be a confusing and incomplete model that has led to varying degrees of misunderstanding about heterochrony among evolutionary biologists. Much of the confusion exists because the model is explicitly limited to phylogenetic patterns (interspecific comparisons), but has been used for intraspecific comparisons. Because heterochrony may underlie all morphological variation and possibly is the developmental phenomenon producing all morphological change it is important that descriptions of heterochronic patterns and processes be clear and precise over all levels of analysis. To this end we discuss and clarify the previous model for heterochrony, reject some of the terminology and suggest alternatives, and then expand the model to include a new nomenclature for intraspecific heterochronic phenomena. Our modifications are essential to maintain the critical conceptual distinction between inter- vs. intraspecific heterochronic patterns and processes in evolutionary biology.
The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.
Recently a growing number of biologists have begun to consider the causal role that processes of embryonic development may play in evolution. This constitutes a reunion of these phenomena which had been linked in the nineteenth century through Haeckel's biogenetic law. This reunion may result in a new subdiscipline of biology, if there is a set of unique concepts and methods which tie the various research approaches together. Such concepts as bauplan, canalization, and developmental constraint, may serve in such a capacity. The methods employed must combine comparative and experimental analyses, with special attention paid to the range of variation in developmental events within each taxon. These concepts and methods are also applicable to the problem of how development evolved, thus the evolution of development may also be considered part of the reunion. The reunion is discussed in terms of the potential participation of various schools of thought found in the current literature.
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.
The lineage and fate of each blastomere in the 32-cell embryo of the direct-developing sea urchin Heliocidaris erythrogramma have been traced by microinjection of tetramethylrhodamine-dextran. The results reveal substantive evolutionary modifications of the ancestral cell lineage pattern of indirect sea urchin development. Significant among these modifications are changes in the time and order of cell lineage segregation: vegetal ectodermal founder cells consistently arise earlier than during indirect development, while internal founder cells generally segregate later and in a different sequence. Modifications have also arisen in proportions of the embryo fated to become various cell types and larval structures. Ectodermal fates, particularly vestibular ectoderm, comprise a greater proportion of the total cellular volume in H. erythrogramma. Among internal cell types, coelom consumes more and endoderm less of the remaining cellular volume than during indirect sea urchin development. Evolutionary modifications are also apparent in the positional origin of larval cell types and structures in H. erythrogramma. These include an apparent tilt in the axis of prospective cell fate relative to the animal-vegetal axis as defined by cleavage planes. Together these evolutionary changes in the cell lineage of H. erythrogramma produce an accelerated loss of dorsoventral symmetry in cell fate relative to indirect development. The extent and diversity of rearrangements in its cell lineage indicate that the nonfeeding larva of H. erythrogramma is a highly modified, novel form rather than a degenerate pluteus larva. These same modifications underscore the evolutionarily flexible relationship between cell lineage, gene expression, and larval morphology in sea urchin development.
To investigate jaw evolution in beloniform fishes, we reconstructed the phylogeny of 54 species using fragments of two nuclear
(RAG2 and Tmo-4C4) and two mitochondrial (cytochrome b and 16S rRNA) genes. Our total molecular evidence topology refutes
the monophyly of needlefishes (Belonidae) and halfbeaks (Hemiramphidae), but supports the monophyly of flyingfishes (Exocoetidae)
and sauries (Scomberesocidae). Flyingfishes are nested within halfbeaks, and sauries are nested within needlefishes. Optimization
of jaw characters on the tree reveals a diverse array of evolutionary changes in ontogeny. During their development, needlefishes
pass through a “halfbeak” stage that closely resembles the adult condition in the hemiramphid halfbeaks. The reconstruction
of jaw transitions falsifies the hypothesis that halfbeaks are paedomorphic derivatives of needlefishes. Instead, halfbeaks
make up a basal paraphyletic grade within beloniforms, and the needlefish jaw morphology is relatively derived. The parallel
between needlefish ontogeny and beloniform phylogeny is discussed, and clades amenable to future morphological analysis are
proposed.
Many evolutionary modifications in development and life history derive from changes in embryonic gene expression. However, the genetic variation affecting gene expression in natural populations is not well understood, nor are the evolutionary mechanisms that operate on that variation. The early embryonic gene network of the purple sea urchin (Strongylocentrotus purpuratus) has been studied in considerable detail, providing an informative basis for analyzing the developmental and evolutionary mechanisms that alter gene expression. Comparative functional analyses have been carried out for several genes. These case studies indicate a complex relationship between sequence divergence and gene expression: in some cases, gene expression is conserved despite extensive divergence in cis-regulatory sequences, while in others the basis for a change in gene expression does not reside locally but rather in the expression or activity of transcription factors that regulate its expression. Diverse evolutionary mechanisms apparently operate on cis-regulatory regions, including negative, balancing, and stabilizing selection.
Direct development in amphibians is an evolutionarily derived life‐history mode that involves the loss of the free‐living, aquatic larval stage. We examined embryos of the direct‐developing anuran Eleutherodactylus coqui (Leptodactylidae) to evaluate how the biphasic pattern of cranial ontogeny of metamorphosing species has been modified in the evolution of direct development in this lineage. We employed whole‐mount immunohistochemistry using a monoclonal antibody against the extracellular matrix component Type II collagen, which allows visualization of the morphology of cartilages earlier and more effectively than traditional histological procedures; these latter procedures were also used where appropriate. This represents the first time that initial chondrogenic stages of cranial development of any vertebrate have been depicted in whole‐mounts.
Many cranial cartilages typical of larval anurans, e.g., suprarostrals, cornua trabeculae, never form in Eleutherodactylus coqui . Consequently, many regions of the skull assume an adult, or postmetamorphic, morphology from the inception of their development. Other components, e.g., the lower jaw, jaw suspensorium, and the hyobranchial skeleton, initially assume a mid‐metamorphic configuration, which is subsequently remodeled before hatching. Thirteen of the adult complement of 17 bones form in the embryo, beginning with two bones of the jaw and jaw suspensorium, the angulosplenial and squamosal. Precocious ossification of these and other jaw elements is an evolutionarily derived feature not found in metamorphosing anurans, but shared with some direct‐developing caecilians. Thus, in Eleutherodactylus cranial development involves both recapitulation and repatterning of the ancestral metamorphic ontogeny. These modifications, however, are not associated with any fundamental change in adult morphology and cannot at this time be causally linked to the evolutionary success of this extraordinarily speciose genus.
We reviewed the concept of homology, which can broadly be defined as a correspondence between characteristics that is caused by continuity of information (Van Valen 1982). The concept applies widely in molecular biology when correspondence is taken to mean a genetic relationship resulting from a unique heritable modification of a feature at some previous point in time. Such correspondence can be established for features within a single organism as well as between organisms, making paralogy a valid form of molecular homology under this definition. Molecular homology can be recognized at a variety of organizational levels, which are interdependent. For example, the recognition of homology at the site level involves a statement of homology at the sequence level, and vice versa. This hierarchy, the potential for nonhomologous identity at the site level, and such processes as sequence transposition combine to yield a molecular equivalent to complex structural homology at the anatomical level. As a result, statements of homology between heritable units can involve a valid sense of percent homology. We analyzed DNA hybridization with respect to the problems of recognizing homology and using it in phylogenetic inference. Under a model requiring continuous divergence among compared sequences, DNA hybridization distances embed evolutionary hierarchy, and groups inferred using pairwise methods of tree reconstruction are based on underlying patterns of apomorphic homology. Thus, symple-siomorphic homology will not confound DNA hybridization phylogenies. However, nonhomologous identities that act like apomorphic homologies can lead to inaccurate reconstructions. The main difference between methods of phylogenetic analysis of DNA sequences is that parsimony methods permit hypotheses of nonhomology, whereas distance methods do not.
Adultation is a heterochronic mode of development in which adult tissues and organs differentiate precociously during the larval phase. We have investigated the expression of an adult muscle actin gene during adultation in the ascidian Molgula citrina. Ascidians contain multiple muscle actin genes which are expressed in the larva, the adult, or during both phases of the life cycle. In ascidian species with conventional larval development, the larval mesenchyme cells, which are believed to be progenitors of the adult mesoderm, remain undifferentiated and do not express the muscle actin genes. In M. citrina, the mesenchyme cells differentiate precociously during larval development, suggesting a role in adultation. An adult muscle actin gene from M. citrina was obtained by screening a mantle cDNA library with a probe containing the coding region of SpMA1, a Styela plicata adult muscle actin gene. The screen yielded a cDNA clone designated McMA1, which contained virtually the complete coding and 3' noncoding regions of a muscle actin gene. The deduced McMA1 and SpMA1 proteins exhibit 97% identity in amino acid sequence and may be encoded by homologous genes. The McMA1 gene is expressed in juveniles and adults, but not in larval tail muscle cells, suggesting that it is an adult muscle actin gene. In situ hybridization with a 3' non-coding region probe was used to determine whether the McMA1 gene is expressed during adultation in M. citrina. McMA1 mRNA was first detected exclusively in the mesenchyme cells during the late tailbud stage and continued to accumulate in these cells during their migration into the future body cavity and heart primordium in the hatched larva. The McMA1 transcripts persisted in mesenchyme cells after larval metamorphosis. It is concluded that an adult muscle actin gene shows a heterochronic shift of expression into the larval phase during adultation in M. citrina.
We describe an evolutionary comparison of expression of the actin gene families of two congeneric sea urchins. Heliocidaris tuberculata develops indirectly via a planktonic feeding pluteus that forms a juvenile rudiment after a long period of larval development. H. erythrogramma is a direct developer that initiates formation of a juvenile rudiment immediately following gastrulation. The developmental expression of each actin isoform of both species was determined by in situ hybridization. The observed expression patterns are compared with known expression patterns in a related indirect-developing sea urchin, Strongylocentrotus purpuratus. Comparisons reveal unexpected patterns of conserved and divergent expression. Cytoplasmic actin, CyIII, is expressed in the aboral ectoderm cells of the indirect developers, but is an unexpressed pseudogene in H. erythrogramma, which lacks aboral ectoderm. This change is correlated with developmental mode. Two CyII actins are expressed in S. purpuratus, and one in H. erythrogramma, but no CyII is expressed in H. tuberculata despite its great developmental similarity to S. purpuratus. CyI expression differs slightly between Heliocidaris and Strongylocentrotus with more ectodermal expression in Heliocidaris. Evolutionary changes in actin gene expression reflect both evolution of developmental mode as well as a surprising flexibility in gene expression within a developmental mode.
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.
Sea urchins have long been used to study morphogenesis and cell fate specification and are an established model system in
developmental biology (1). Most contemporary studies have focused on early development, however, and few molecular genetic studies have examined larval
development, or the formation of the highly derived radial body plan of the adult (2). A better understanding of the molecular genetic basis of both the body plans of this phylum may contribute significantly
to several fields of biology (3,4).
This chapter discusses the current understanding of mechanisms that underlie the patterning of the early sea urchin embryo. Its focus is on the partitioning of the cleavage and blastula stage embryo into distinct domains of gene expression and cell fate. Although many questions remain unanswered, recent studies have advanced the understanding of the early patterning of this embryo, and so a re-evaluation of the problem is warranted. The sea urchin embryo has a long and rich history as a model system for the analysis of patterning. The classical fate map of the cleavage stage embryo (Hörstadius, 1973) has been modified in important ways by recent studies. Improved methods of cell labeling have been used to generate higher resolution fate maps and have made it possible to examine more advanced developmental stages. The most extensive fate mapping studies have been carried out with embryos of Lytechinus variegatus and Strongylocentrotus purpuratus.
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.
The study of mammalian evolution often relies on detailed analysis of dental morphology. For molecular patterning to play a role in dental evolution, gene expression differences should be linkable to corresponding morphological differences. Because teeth, like many other structures, are complex and evolution of new shapes usually involves subtle changes, we have developed topographic methods by using Geographic Information Systems. We investigated how genetic markers for epithelial signaling centers known as enamel knots are associated with evolutionary divergence of molar teeth in two rodent species, mouse and vole. Our analysis of expression patterns of Fgf4, Lef1, p21, and Shh genes in relation to digital elevation models of developing tooth shapes shows that molecular prepatterns predict the lateral cusp topography more than a day in advance. A heterotopic shift in the molecular prepatterns can be implicated in the evolution of mouse molar, changing locations from which historically homologous cusps form. The subtle but measurable heterotopic shifts may play a large role in the evolution of tooth cusp topographies. However, evolutionary increase in the number of longitudinal cusps in vole molar has involved accelerated longitudinal growth and iterative addition of new cusps without changes in lateral cusp topography. The iterative addition of cusps after the establishment of lateral cusp topography may limit the independence of individual morphological features used in evolutionary studies. The diversity of mammalian molar patterns may largely result from the heterotopic and iterative processes.
Modularity is a salient feature of development and crucial to its evolution. This paper extends modularity to include the concept of gene expression territory, as established for sea urchin embryos. Territories provide a mechanism for partitioning of the cells of a rapidly developing embryo into functional units of a feeding larva. Territories exhibit the characteristics of modules. The paper asks if the embryo and the nonfeeding larva of the direct-developing sea urchin Heliocidaris erythrogramma are organized into gene expression territories, and if its territories correspond to the canonical territories of the pluteus. An analysis of cell lineage and gene expression data for H. erythrogramma shows that skeletogenic cell, coelomic, and vegetal plate gene expression territories are conserved, although they arise from cell lineages distinct from those of the pluteus, and the overall morphology of the larva differs from that of a pluteus. The ectoderm, as in indirect developers, is divided into territories. However, the oral ectodermal territory characteristic of the pluteus is absent in H. erythrogramma. Oral ectoderm is restored in hybrids of H. erythrogramma eggs fertilized by Heliocidaris tuberculata sperm. This indicates that embryonic modules evolve by changes in expression of dominant regulatory genes within territories and that entire modules can be eliminated in evolution of embryos.
ResearchGate has not been able to resolve any references for this publication.