Origins of the other metazoan body plans: the evolution of larval forms

Bilaterian animal body plan origins are not solely about adult forms. Most animals have larvae with body plans, ontogenies and ecologies distinct from adults. There are two primary hypotheses for larval origins. The first hypothesis suggests that the first animals were small pelagic forms similar to modern larvae, with adult bilaterian body plans evolved subsequently. The second hypothesis suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolation of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. If primitive metazoans were like modern larvae and distinct adult forms evolved independently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morphological convergence, but with distinct patterning genes, and this is observed. Thus, comparative studies of gene expression support independent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as being primitive, with planktonic larvae arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.     

Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs.

The Puerto Rican direct-developing frog Eleutherodactylus coqui (Leptodactylidae) displays a novel mode of jaw muscle development for anuran amphibians. Unlike metamorphosing species, several larval-specific features never form in E. coqui; embryonic muscle primordia initially assume an abbreviated, mid-metamorphic configuration that is soon remodelled to form the adult morphology before hatching. Also lacking are both the distinct population of larval myofibres and the conspicuous, larval-to-adult myofibre turnover that are characteristic of muscle development in metamorphosing species. These modifications are part of a comprehensive alteration in embryonic cranial patterning that has accompanied life history evolution in this highly speciose lineage. Embryonic ''repatterning'' in Eleutherodactylus may reflect underlying developmental mechanisms that mediate the integrated evolution of complex structures. Such mechanisms may also facilitate, in organisms with a primitively complex life cycle, the evolutionary dissociation of embryonic, larval, and adult features.     

Developmental palaeontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives

The study of fossilized ontogenies in mammals is mostly restricted to postnatal and late stages of growth, but nevertheless can deliver great insights into life history and evolutionary mechanisms affecting all aspects of development. Fossils provide evidence of developmental plasticity determined by ecological factors, as when allometric relations are modified in species which invaded a new space with a very different selection regime. This is the case of dwarfing and gigantism evolution in islands. Skeletochronological studies are restricted to the examination of growth marks mostly in the cement and dentine of teeth and can provide absolute age estimates. These, together with dental replacement data considered in a phylogenetic context, provide life-history information such as maturation time and longevity. Palaeohistology and dental replacement data document the more or less gradual but also convergent evolution of mammalian growth features during early synapsid evolution. Adult phenotypes of extinct mammals can inform developmental processes by showing a combination of features or levels of integration unrecorded in living species. Some adult features such as vertebral number, easily recorded in fossils, provide indirect information about somitogenesis and hox-gene expression boundaries. Developmental palaeontology is relevant for the discourse of ecological developmental biology, an area of research where features of growth and variation are fundamental and accessible among fossil mammals.     

Who came first--larvae or adults? origins of bilaterian metazoan larvae

There is a classic controversy in zoology over whether the common ancestor of living bilaterian phyla was a benthic animal with a bilaterian body plan, or was a pelagic larva-like animal similar to what we see today in the primary larvae of indirect-developing bilaterians. We examine the current larva-like adult hypothesis, and present an alternate model for the evolution of complex life histories by intercalation of larval features into the ontogeny of an ancestral direct-developing bilaterian. This gradual accumulation of larval features results in a developmental regulatory program that produces a larva distinct in body plan from the adult. The evolution of a rapid and complete metamorphosis is made possible by the convergent evolution of set aside cells in the final stages of the emergence of indirect developing larval forms. Although convergences abound either hypothesis for the evolution of developmental pathways and life histories, the bilaterian first hypothesis is consistent with all stages of evolution of a complex life history being selectively advantageous, with the rapid evolution of larval forms, and with the frequent co-option of genes from the adult phase of the life cycle prevalent in the evolution of embryos and larvae.     

Postnatal Cranial Development in Papionin Primates: An Alternative Model for Hominin Evolutionary Development

The evolution of hominin growth and life history has long been a subject of intensive research, but it is only recently that paleoanthropologists have considered the ontogenetic basis of human morphological evolution. To date, most human EvoDevo studies have focused on developmental patterns in extant African apes and humans. However, the Old World monkey tribe Papionini, a diverse clade whose members resemble hominins in their ecology and population structure, has been proposed as an alternative model for human craniofacial evolution. This paper reviews prior studies of papionin development and socioecology and presents new analyses of juvenile shape variation and ontogeny to address fundamental questions concerning primate cranial development, including: (1) When are cranial shape differences between species established? (2) How do epigenetic influences modulate early-arising pattern differences? (3) How much do postnatal developmental trajectories vary? (4) What is the impact of developmental variation on adult cranial shape? and, (5) What role do environmental factors play in establishing adult cranial form? Results of this inquiry suggest that species differences in cranial morphology arise during prenatal or earliest postnatal development. This is true even for late-arising features that develop under the influence of epigenetic factors such as mechanical loading. Papionins largely retain a shared, ancestral pattern of ontogenetic shape change, but large size and sexual dimorphism are associated with divergent developmental trajectories, suggesting differences in cranial integration. Developmental simulation studies indicate that postnatal ontogenetic variation has a limited influence on adult cranial morphology, leaving early morphogenesis as the primary determinant of cranial shape. The ability of social factors to influence craniofacial development in Mandrillus suggests a possible role for phentotypic plasticity in the diversification of primate cranial form. The implications of these findings for taxonomic attribution of juvenile fossils, the developmental basis of early hominin characters, and hominin cranial diversity are discussed.     

Homology and the evolution of novelty during Danio adult pigment pattern development

Recent studies using zebrafish and its relatives have provided insights into the development and evolution of adult pigment patterns. In this review, I describe how an iterative approach using a biomedical model organism and its close relatives can be used to elucidate both mechanistic and organismal aspects of pigment pattern formation. Such analyses have revealed critical roles for post-embryonic latent precursors as well as interactions among different pigment cell classes during adult pigment pattern formation and diversification. These studies also have started to reveal homologous and novel features of the underlying developmental processes.     

A novel ontogenetic pathway in hybrid embryos between species with different modes of development

To investigate the bases for evolutionary changes in developmental mode, we fertilized eggs of a direct-developing sea urchin, Heliocidaris erythrogramma, with sperm from a closely related species, H. tuberculata, that undergoes indirect development via a feeding larva. The resulting hybrids completed development to form juvenile adult sea urchins. Hybrids exhibited restoration of feeding larval structures and paternal gene expression that have been lost in the evolution of the direct-developing maternal species. However, the developmental outcome of the hybrids was not a simple reversion to the paternal pluteus larval form. An unexpected result was that the ontogeny of the hybrids was distinct from either parental species. Early hybrid larvae exhibited a novel morphology similar to that of the dipleurula-type larva typical of other classes of echinoderms and considered to represent the ancestral echinoderm larval form. In the hybrid developmental program, therefore, both recent and ancient ancestral features were restored. That is, the hybrids exhibited features of the pluteus larval form that is present in both the paternal species and in the immediate common ancestor of the two species, but they also exhibited general developmental features of very distantly related echinoderms. Thus in the hybrids, the interaction of two genomes that normally encode two disparate developmental modes produces a novel but harmonious ontongeny.     

Evolution of pelagic direct development in the starfish Pteraster tesselatus (Asteroidea: Velatida)

Despite a diversity of larval forms, remarkably conservative features of asteroid development define a larval body plan that occurs throughout the class. However, recent work on the starfish Pteraster tesselatus has documented a highly derived pattern of development. Several features, including radial symmetry, parallel embryonic and adult axes of symmetry, absence of a preoral lobe, and formation of coeloms in the adult orientation from seven separate enterocoels, have not been reported in asteroids before. The complete absence of the larval body plan features that are found in other asteroids, indicates that P. tesselatus develops directly from the embryo to the juvenile and has a pelagic, nonfeeding (lecithotrophic), but nonlarval mode of development. I postulate that direct development evolved over an extended period in a lineage of brooding, deep-sea velatid (probably pterastcrid) ancestors of P. tesselatus. Selection for increased developmental efficiency (loss of nonfunctional larval features) in the brooded offspring, could explain the lack of larval settlement structures, the nonlarval arrangement of coeloms, the lack of a preoral lobe, the transverse orientation of the juvenile disc, and the lack of bilateral symmetry. The pattern of coclomogenesis could have been derived from that of other velatids (e.g. solasterids) by relatively simple changes in timing and orientation of entcroeoel formation. Rotation and posterior translation of the coelomic fate map of the archenteron prior to enlerocoel formation would produce the coelomic compartments in the adult orientation that characterizes direct development in P. tesselatus. These unusual developmental features lead to a radically different interpretation for the evolution of the pelagic ‘larva’ of P. tesselatus: (1) evolution of benthie brooding, (2) extreme simplification of development involving the loss of all larval features from the life cycle, and (3) subsequent re-evolution of pelagic development. In the case of P. tesselatus, where all larval structures were lost, there do not seem to be functional constraints preventing the re-evolution of pelagic development. Analysis of pelagic and benthie larvae, in other asteroids, suggests that major ecological transitions in life histories need not be associated with substantia] changes in morphology. The loss of pelagic development should have occurred repeatedly and should be readily reversible. These findings have interesting implications for the loss and evolution of pelagic dispersal in the life histories of marine benthie invertebrates.     

Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies

Evolution can be viewed as a series of changes in the developmental program along the phylogenetic tree. To better understand the early evolution of the vertebrate skull, we can use the embryos of the cyclostome species as models. By comparing the cyclostome developmental patterns with those of gnathostomes, it becomes possible to distinguish the primitive and derived parts of the developmental program as taxon-specific traits. These traits are often recognizable as developmental constraints that define taxa by biasing the developmental trajectories within a certain limited range, resulting in morphological homologies in adults. These developmental constraints are distributed on the phylogenetic tree like the morphological character states of adult animals and are associated with specific regions of the tree. From this perspective, we emphasize the importance of considering gene expression and embryonic anatomy as the mechanistic bases that can result in homologous or nonhomologous morphological patterns at later developmental stages. Taking the acquisition of the jaw and trabecula cranii as examples, we demonstrate that a set of embryonic features can be coupled or decoupled during evolution and development. When they are coupled, they exert an ancestral developmental constraint that results in homologous morphological patterns, and when they are decoupled, the ancestral constraints tend to be abandoned, generating a new body plan. The heterotopy behind the specification of the oral domain is an example of decoupling, based on shifted tissue interactions. We also stress the importance of "developmental burden" in determining the sequential order of changes through evolution.     

Rates of Evolution in Developmental Processes

The tempo and mode of morphological evolution are influencedby several factors, among which evolutionary transformationsin developmental processes are likely to be important. Comparingthe embryos of extant species in an explicit phylogenetic framwork allows the estimation of minimum average rates of evolutionin quantitative developmental parameters. It also allows delineationof the maximum time that complex qualitative transformationsin developmental mechanism take to evolve. This paper analyzesrates of quantitative and qualitative developmental evolutionusing examples drawn primarily from echinoderms. The resultsdemonstrate that rates of developmental evolution can be comparableto rates of morphological evolution. There is no indicationthat rates of evolution in development are lower for earlierstages, contrary to the prediction of "tree" models of epigeneticinteractions. In particular, rates of evolution in oogenesiscan exceed rates of evolution in adult body size. Rates of developmentalevolution can vary by up to two orders of magnitude within aclade. Whether such large scale variation in evolutionary ratesof developmental processes is a general phenomenon can onlybe answered by further study.     

Parasites affect song complexity and neural development in a songbird

There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Here, we show that adult male canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibit reduced development of the high vocal centre (HVC) song nucleus in the brain. Our results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behaviour. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton-Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.     

Frogs without polliwogs: evolution of anuran direct development

Direct development is the assumption of the adult morphology without progression through an intervening, morphologically distinct, free-living larval phase. We discuss the ecological factors contributing to the evolution of this derived life-history strategy in frogs, and the developmental modifications that facilitate such an unusual mode of embryogenesis. Studies on the Puerto Rican tree frog, Eleutherodactylus coqui, have identified several such modifications, including developmental adaptations for dealing with increased egg size, and loss of tadpole structures. Surprisingly, this direct developer still undergoes a thyroid hormone-dependent metamorphosis, which occurs before hatching. We suggest how the ancestral biphasic developmental pattern may have been rearranged during the evolution of direct development.     

SEASONALITY MAINTAINS ALTERNATIVE LIFE‐HISTORY PHENOTYPES

Many organisms express discrete alternative phenotypes (polyphenisms) in relation to predictable environmental variation. However, the evolution of alternative life‐history phenotypes remains poorly understood. Here, we analyze the evolution of alternative life histories in seasonal environments by using temperate insects as a model system. Temperate insects express alternative developmental pathways of diapause and direct development, the induction of a certain pathway affecting fitness through its life‐history correlates. We develop a methodologically novel and holistic simulation model and optimize development time, growth rate, body size, reproductive effort, and adult life span simultaneously in both developmental pathways. The model predicts that direct development should be associated with shorter development time (duration of growth) and adult life span, higher growth rate and reproductive effort, smaller body size as well as lower fecundity compared to the diapause pathway, because the two generations divide the available time unequally. These predictions are consistent with many empirical data. Our analysis shows that seasonality alone can explain the evolution of alternative life histories.     

Ontogenetic diversity of colonies and intercellular cytoplasmic bridges in the algae of the genus Volvox

In all representatives of the genus Volvox, cells of cleaving embryos are connected by cytoplasmic bridges, which play an important role in the process of young colony inversion. However, during subsequent development, the intercellular bridges are retained not in all species of Volvox; the occurrence of the bridges in an adult colony correlates with the small size of mature gonidia (asexual reproductive cells) and with the presence of cell growth in the intervals between divisions. This complex of ontogenetic features is derived and arises independently in three evolutionary lineages of colonial volvocine algae. A putative role of the syncytial state of adult colonies for the evolution of developmental cycles in Volvox is discussed.     

Cranial ontogeny of Papio baboons (Papio hamadryas)

Cranial form in subspecies of Papio baboons (Papio hamadryas) varies in relation to size, geography, and sex. However, knowledge about this variation is based mainly on adults, precluding direct assessments of the evolutionary factors that are ultimately responsible for adult shape variation. Consequently, this study tests hypotheses about the development of size and shape differences among subspecies of Papio baboons, anticipating limited evolutionary divergences in the ontogenetic pathways leading to adult endpoints. Geometric morphometric and bivariate allometric analyses are used to explore developmental size and shape variation. Allometric scaling in adult Papio baboons occurs because both sexes and all subspecies follow similar developmental pathways to a variety of adult forms. However, complex allometry contributes to form differences, producing potentially important shape differences that emerge during development. Modest shape differences that are statistically independent of size distinguish chacma baboons (P. h. ursinus) from other forms. A small-headed subspecies, the Kinda baboon (P. h. kindae), also presents a distinctive ontogeny, and may provide insights into the evolution of size change in this species. Variation among subspecies that is statistically independent of size involves the rostrum, zygomatic breadths, and cranial flexion. These features may be related to diet, but the precise biomechanical correlates of baboon form variation remain unclear.     

Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning

The investigation of neurogenesis in polychaetes not only facilitates insights into the developmental biology of this group, but also provides new data for phylogenetic analyses. This should eventually lead toward a better understanding of metazoan evolution including key issues such as the ontogenetic processes that underlie body segmentation. We here document the development of the larval nervous system in the polychaete Sabellaria alveolata using fluorescence-coupled antibodies directed against serotonin, FMRFamide, and tubulin in combination with confocal laser scanning microscopy and 3D reconstruction software. The overall pattern of neurogenesis in S. alveolata resembles the condition found in other planktonic polychaete trochophores where the larval neural body plan including a serotonergic prototroch nerve ring is directly followed by adult features of the nervous system such as circumesophageal connectives and paired ventral nerve cords. However, distinct features are also found in S. alveolata, such as the innervation of the apical organ with ring-shaped neurons, the low number of immunoreactive perikarya, and the lack of a posterior serotonergic cell. Moreover, in the larvae of S. alveolata, two distinct modes of neuronal development are expressed, viz. the simultaneous formation of the first three segmental neurons of the peripheral nervous system on the one hand versus the sequential appearance of the ventral commissures on the other. This highlights the complex mechanisms that underlie annelid body segmentation and indicates divergent developmental pathways within polychaete annelids that lead to the segmented nervous system of the adult.     

Written in stone: fossils, genes and evo-devo

Fossils give evo-devo a past. They inform phylogenetic trees to show the direction of evolution of developmental features, and they can reveal ancient body plans. Fossils also provide the primary data that are used to date past events, including divergence times needed to estimate molecular clocks, which provide rates of developmental evolution. Fossils can set boundaries for hypotheses that are generated from living developmental systems, and for predictions of ancestral development and morphologies. Finally, although fossils rarely yield data on developmental processes directly, informative examples occur of extraordinary preservation of soft body parts, embryos and genomic information.     

Developing the genotype-to-phenotype relationship in evolutionary theory: A primer of developmental features

For decades, there have been repeated calls for more integration across evolutionary and developmental biology. However, critiques in the literature and recent funding initiatives suggest this integration remains incomplete. We suggest one way forward is to consider how we elaborate the most basic concept of development, the relationship between genotype and phenotype, in traditional models of evolutionary processes. For some questions, when more complex features of development are accounted for, predictions of evolutionary processes shift. We present a primer on concepts of development to clarify confusion in the literature and fuel new questions and approaches. The basic features of development involve expanding a base model of genotype-to-phenotype to include the genome, space, and time. A layer of complexity is added by incorporating developmental systems, including signal-response systems and networks of interactions. The developmental emergence of function, which captures developmental feedbacks and phenotypic performance, offers further model elaborations that explicitly link fitness with developmental systems. Finally, developmental features such as plasticity and developmental niche construction conceptualize the link between a developing phenotype and the external environment, allowing for a fuller inclusion of ecology in evolutionary models. Incorporating aspects of developmental complexity into evolutionary models also accommodates a more pluralistic focus on the causal importance of developmental systems, individual organisms, or agents in generating evolutionary patterns. Thus, by laying out existing concepts of development, and considering how they are used across different fields, we can gain clarity in existing debates around the extended evolutionary synthesis and pursue new directions in evolutionary developmental biology. Finally, we consider how nesting developmental features in traditional models of evolution can highlight areas of evolutionary biology that need more theoretical attention.     

THE EVOLUTION OF CANALIZATION AND THE BREAKING OF VON BAER'S LAWS: MODELING THE EVOLUTION OF DEVELOPMENT WITH EPISTASIS

Evolution can change the developmental processes underlying a character without changing the average expression of the character itself. This sort of change must occur in both the evolution of canalization, in which a character becomes increasingly buffered against genetic or developmental variation, and in the phenomenon of closely related species that show similar adult phenotypes but different underlying developmental patterns. To study such phenomena, I develop a model that follows evolution on a surface representing adult phenotype as a function of underlying developmental characters. A contour on such a “phenotype landscape” is a set of states of developmental characters that produce the same adult phenotype. Epistasis induces curvature of this surface, and degree of canalization is represented by the slope along a contour. I first discuss the geometric properties of phenotype landscapes, relating epistasis to canalization. I then impose a fitness function on the phenotype and model evolution of developmental characters as a function of the fitness function and the local geometry of the surface. This model shows how canalization evolves as a population approaches an optimum phenotype. It further shows that under some circumstances, “decanalization” can occur, in which the expression of adult phenotype becomes increasingly sensitive to developmental variation. This process can cause very similar populations to diverge from one another developmentally even when their adult phenotypes experience identical selection regimes.     

Larval legs of mulberry silkworm Bombyx mori are prototypes for the adult legs

Morphological diversity of leg appendages is one of the hallmarks of developmental evolution. Limbs in insects may develop either from their embryonic prototypes or from imaginal discs harbored inside the larva. Bombyx mori (B. mori), a Lepidopteran insect, develops adult wings from larval wing imaginal discs. However, it has been debated whether the adult legs of B. mori arise from imaginal discs or from the larval legs. Here we addressed how the larval legs relate to their adult counterparts. We present the morphological landmarks during early leg development. We used expression of developmental genes like Distalless and extradenticle to mark leg primordia. Finally, we employed classical excision approach to develop a fate map of the adult leg. Excision and ablation of thoracic legs along proximo-distal axis at various times during larval development resulted in the loss of corresponding adult leg segments. Our data suggest that B. mori legs develop from larval appendages rather than leg imaginal discs.