A developmental basis for the Cambrian radiation

As extant bilaterian phyla emerged during the Lower Cambrian, these clades acquired morphological features that separated them from their stem groups. At the same time, morphological variants on the body plan within a phylum emerged that we recognize as classes and subphyla. In many cases, the emergence of body plan variants within a phylum is associated with major changes in patterns of early regional specification. Subsequently these different patterns of regional specification were stabilized, probably because later developmental events depended on them. As a consequence, the frequency of new body plan variants involving early development declined in these lineages at later periods during their history. This hypothesis is explicated here by examining the process of early regional specification in the different subphyla of brachiopods and in pairs of species from the same subphylum belonging to different clades that originated during the Jurassic, Ordovician, and Lower Cambrian.     

THE IMPORTANCE OF PREADAPTED GENOMES IN THE ORIGIN OF THE ANIMAL BODYPLANS AND THE CAMBRIAN EXPLOSION

The genomes of taxa whose stem lineages branched early in metazoan history, and of allied protistan groups, provide a tantalizing outline of the morphological and genomic changes that accompanied the origin and early diversifications of animals. Genome comparisons show that the early clades increasingly contain genes that mediate development of complex features only seen in later metazoan branches. Peak additions of protein‐coding regulatory genes occurred deep in the metazoan tree, evidently within stem groups of metazoans and eumetazoans. However, the bodyplans of these early‐branching clades are relatively simple. The existence of major elements of the bilaterian developmental toolkit in these simpler organisms implies that these components evolved for functions other than the production of complex morphology, preadapting the genome for the morphological differentiation that occurred higher in metazoan phylogeny. Stem lineages of the bilaterian phyla apparently required few additional genes beyond their diploblastic ancestors. As disparate bodyplans appeared and diversified during the Cambrian explosion, increasing complexity was accommodated largely through changes in cis‐regulatory networks, accompanied by some additional gene novelties. Subsequently, protein‐coding genic richness appears to have essentially plateaued. Some genomic evidence suggests that similar stages of genomic evolution may have accompanied the rise of land plants.     

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.     

Ecological innovations in the Cambrian and the origins of the crown group phyla

Simulation studies of the early origins of the modern phyla in the fossil record, and the rapid diversification that led to them, show that these are inevitable outcomes of rapid and long-lasting radiations. Recent advances in Cambrian stratigraphy have revealed a more precise picture of the early bilaterian radiation taking place during the earliest Terreneuvian Series, although several ambiguities remain. The early period is dominated by various tubes and a moderately diverse trace fossil record, with the classical ‘Tommotian’ small shelly biota beginning to appear some millions of years after the base of the Cambrian at ca 541 Ma. The body fossil record of the earliest period contains a few representatives of known groups, but most of the record is of uncertain affinity. Early trace fossils can be assigned to ecdysozoans, but deuterostome and even spiralian trace and body fossils are less clearly represented. One way of explaining the relative lack of clear spiralian fossils until about 536 Ma is to assign the various lowest Cambrian tubes to various stem-group lophotrochozoans, with the implication that the groundplan of the lophotrochozoans included a U-shaped gut and a sessile habit. The implication of this view would be that the vagrant lifestyle of annelids, nemerteans and molluscs would be independently derived from such a sessile ancestor, with potentially important implications for the homology of their sensory and nervous systems.     

Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan

Echinoderms are unique among animal phyla in having a pentaradial body plan, and their fossil record provides critical data on how this novel organization came about by revealing intermediate stages. Here, we report a spiral-plated animal from the early Cambrian of Morocco that is the most primitive pentaradial echinoderm yet discovered. It is intermediate between helicoplacoids (a bizarre group of spiral-bodied echinoderms) and crown-group pentaradiate echinoderms. By filling an important gap, this fossil reveals the common pattern that underpins the body plans of the two major echinoderm clades (pelmatozoans and eleutherozoans), showing that differential growth played an important role in their divergence. It also adds to the striking disparity of novel body plans appearing in the Cambrian explosion.     

The Radiata and the evolutionary origins of the bilaterian body plan

The apparent conservation of cellular and molecular developmental mechanisms observed in a handful of bilaterian metazoans has spawned a "race" to reconstruct the bilaterian ancestor. Knowledge of this ancestor would permit us to reconstruct the evolutionary changes that have occurred along specific bilaterian lineages. However, comparisons among extant bilaterians provide an unnecessarily limited view of the ancestral bilaterian. Since the original bilaterians are believed by many to be derived from a radially symmetrical ancestor, additional evidence might be obtained by examining present-day radially symmetrical animals. We briefly review pertinent features of the body plans of the extant radial eumetazoan phyla, the Cnidaria, and Ctenophora, in the context of revealing potential evolutionary links to the bilaterians.     

Evo-devo: variations on ancestral themes

Most animals evolved from a common ancestor, Urbilateria, which already had in place the developmental genetic networks for shaping body plans. Comparative genomics has revealed rather unexpectedly that many of the genes present in bilaterian animal ancestors were lost by individual phyla during evolution. Reconstruction of the archetypal developmental genomic tool-kit present in Urbilateria will help to elucidate the contribution of gene loss and developmental constraints to the evolution of animal body plans.     

Vestiges of a beginning? Paleontological and geochemical constraints on early animal evolution

Inspired by molecular clock estimates, some biologists have proposed that animals in general, and bilaterian metazoans in particular, began to diverge substantially earlier than fossils indicate. Balavoine and Adoutte [Science 280 (1998) 397] specifically hypothesized that the Cambrian explosion documents parallel radiations within three major bilaterian clades that diverged from one another relatively early in the Neoproterozoic Era. The geological record is permissive with respect to such hypotheses, but not encouraging. The earliest evolution of animals certainly took place before the initial appearance of phosphatic animal microfossils or Ediacaran macrofossils, but bilaterian clades need not have been part of this metazoan “pre-history”. Alternatively, the evolution of large size, made possible by late Neoproterozoic oxygen increase, may have provided the selective environment in which stem bilaterians differentiated. Cambrian events per se appear to have begun in the wake of environmental perturbation and accompanying extinction near the Proterozoic–Cambrian boundary.     

Patterns of cranial shape diversification during the phylogenetic branching process of New World monkeys (Primates: Platyrrhini)

One of the central topics in evolutionary biology is understanding the processes responsible for phenotypic diversification related to ecological factors. New World monkeys are an excellent reference system to investigate processes of diversification at macroevolutionary scales. Here, we investigate the cranial shape diversification related to body size and ecology during the phylogenetic branching process of platyrrhines. To investigate this diversification, we used geometric morphometric techniques, a molecular phylogenetic tree, ecological data and phylogenetic comparative methods. Our statistical analyses demonstrated that the phylogenetic branching process is the most important dimension to understand cranial shape variation among extant platyrrhines and suggested that the main shape divergence among the four principal platyrrhine clades probably occurred during the initial branching process. The phylogenetic conservatism, which is the retention of ancestral traits over time within the four principal platyrrhine clades, could be the most important characteristic of platyrrhine cranial shape diversification. Different factors might have driven early shape divergence and posterior relative conservatism, including genetic drift, stabilizing selection, genetic constraints owing to pleiotropy, developmental or functional constraint, lack of genetic variation, among others. Understanding the processes driving the diversification among platyrrhines will probably require further palaeontological, phylogenetic and comparative studies.     

Arthropod body-plan evolution in the Cambrian with an example from anomalocaridid muscle

The ancestor of the arthropods is widely thought to have possessed a hydrostatic skeleton surrounded by peripheral longitudinal and circular musculature, as exhibited by the extant onychophorans. However, the transition to a lever-style musculature system with an articulating exoskeleton poses a difficult problem in functional evolution: did the musculature or the exoskeleton evolve first, and how? Here, by reference to the musculature of the Lower Cambrian stem-group arthropod Pambdelurion, the problem is resolved in terms of preadaptation and functional degeneracy without recourse to saltational notions. Cambrian taxa lying in the stem-groups of the modern phyla may thus be shown to provide unique evidence for the functional progression involved in the assembly of the extant body plans and obviate the need for exotic genetic or developmental mechanisms to explain the evolution of integrated and complex body plans. The notion of the phylum representing a particularly significant level of organization is thereby brought into question.     

Colonial origin for Emetazoa: major morphological transitions and the origin of bilaterian complexity

A new hypothesis for the evolution of Bilateria is presented. It is based on a reinterpretation of the morphological characters shared by protostomes and deuterostomes, which, when taken together with developmental processes shared by the two lineages, lead to the inescapable conclusion that the last common ancestor of Bilateria was complex. It possessed a head, a segmented trunk, and a tail. The segmented trunk was further divided into two sections. A dorsal brain innervated one or more sensory cells, which included photoreceptors. "Appendages" or outgrowths were present. The bilaterian ancestor also possessed serially repeated "segments" that were expressed ontogenetically as blocks of mesoderm or somites with adjoining fields of ectoderm or neuroectoderm. It displayed serially repeated gonads (gonocoels), each with a gonoduct and gonopore to the exterior, and serially repeated "coeloms" with connections to both the gut and the exterior (gill slits and pores). Podocytes, some of which were serially repeated in the trunk, formed sites of ultrafiltration. In addition, the bilaterian ancestor had unsegmented coeloms and a contractile blood vessel or "heart" formed by coelomic myoepithelial cells. These cells and their underlying basement membrane confine the hemocoelic fluid, or blood, in the connective tissue compartment. A possible scenario to account for this particular suite of characters is one in which a colony of organisms with a cnidarian grade of organization became individuated into a new entity with a bilaterian grade of organization. The transformation postulated encompassed three major transitions in the evolution of animals. These transitions included the origins of Metazoa, Eumetazoa, and Bilateria and involved the successive development of poriferan, cnidarian, and bilaterian grades of organization. Two models are presented for the sponge-to-cnidarian transition. In both models the loss of a flow-through pattern of water circulation in poriferans and the establishment of a single opening and epithelia sensu stricto in cnidarians are considered crucial events. In the model offered for the cnidarian-to-bilaterian transition, the last common ancestor of Eumetazoa is considered to have had a colonial, cnidarian-grade of organization. The ancestral cnidarian body plan would have been similar to that exhibited by pennatulacean anthozoans. It is postulated that a colonial organization could have provided a preadaptive framework for the evolution of the complex and modularized body plan of the triploblastic ancestor of Bilateria. Thus, one can explore the possibility that problematica such as ctenophores, the Ediacaran biota, archaeocyaths, and Yunnanozoon reflect the fact that complexity originated early and involved the evolution of a macroscopic compartmented ancestor. Bilaterian complexity can be understood in terms of Beklemishev "cycles" of duplication and colony individuation. Two such cycles appear to have transpired in the early evolution of Metazoa. The first gave rise to a multicellular organism with a sponge grade of organization and the second to the modularized ancestor of Bilateria. The latter episode may have been favored by the ecological conditions in the late Proterozoic. Whatever its cause, the individuation of a cnidarian-grade colony furnishes a possible explanation for the rapid diversification of bilaterians in the late Vendian and Cambrian. The creation of a complex yet versatile prototype, which could be rapidly modified by selection into a profusion of body plans, is postulated to have affected the timing, mode, and extent of the "Cambrian explosion." During the radiations, selective loss or simplification may have been as creative a force as innovation. Finally, colony individuation may have been a unique historical event that imprinted the development of bilaterians as the zootype and phylotypic stage. (ABSTRACT TRUNCATED)     

Morphological and developmental macroevolution: a paleontological perspective

Evidence of the morphological evolution of metazoans has been preserved, in varying degrees of completeness, in the fossil record of the last 600 million years. Although extinction has been incessant at lower taxonomic levels, genomic comparisons among surviving members of higher taxa suggest that much of the developmental systems that pattern their bodyplans has been conserved from early in their history. Comparisons between the origin of morphological disparity in the record and patterns of genomic disparity among living taxa promise to be interesting. For example, Hox cluster composition varies among major taxa, and the fossil record suggests that many of the changes in Hox clusters may have been associated with late Neoproterozoic evolution among minute benthic vermiform clades, from which crown bilaterian phyla arose just before or during the Cambrian explosion. Study of genomic differences among crown classes and orders whosetiming and mode of origin can be inferred from morphological data inthefossil record should throw further light on the timing and mode of origin of genomic disparities.     

Eukaryotic organisms in Proterozoic oceans

The geological record of protists begins well before the Ediacaran and Cambrian diversification of animals, but the antiquity of that history, its reliability as a chronicle of evolution and the causal inferences that can be drawn from it remain subjects of debate. Well-preserved protists are known from a relatively small number of Proterozoic formations, but taphonomic considerations suggest that they capture at least broad aspects of early eukaryotic evolution. A modest diversity of problematic, possibly stem group protists occurs in ca 1800-1300 Myr old rocks. 1300-720 Myr fossils document the divergence of major eukaryotic clades, but only with the Ediacaran-Cambrian radiation of animals did diversity increase within most clades with fossilizable members. While taxonomic placement of many Proterozoic eukaryotes may be arguable, the presence of characters used for that placement is not. Focus on character evolution permits inferences about the innovations in cell biology and development that underpin the taxonomic and morphological diversification of eukaryotic organisms.     

Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form

We examine terminal addition, the process of addition of serial elements in a posterior subterminal growth zone during animal development, across modern taxa and fossil material. We argue that terminal addition was the basal condition in Bilateria, and that modification of terminal addition was an important component of the rapid Cambrian evolution of novel bilaterian morphology. We categorize the often-convergent modifications of terminal addition from the presumed ancestral condition. Our focus on terminal addition and its modification highlights trends in the history of animal evolution evident in the fossil record. These trends appear to be the product of departure from the initial terminal addition state, as is evident in evolutionary patterns within-fossil groups such as trilobites, but is also more generally related to shifts in types of morphologic change through the early Phanerozoic. Our argument is contingent on dates of metazoan divergence that are roughly convergent with the first appearance of metazoan fossils in the latest Proterozoic and Cambrian, as well as on an inference of homology of terminal addition across bilaterian Metazoa.     

The significance of moulting in Ecdysozoan evolution

SUMMARY Three major bilaterian clades first appear in the Early Cambrian fossil record: Deuterostomia, Lophotrochozoa, and Ecdysozoa. The taxa placed in Ecdysozoa are characterized by a moulting habit, unknown in the other major clades. The origin and consequences of moulting are of fundamental importance to the history of the ecdysozoan clade, chiefly because moulting precludes motile ectodermal cilia. Moulting may have originated as an adaptation to permit the enlargement, during growth, of secreted cuticular spines, flanges, and other structures used as ancillary locomotory devices. A combination of phylogenetic and fossil evidence suggests that the early members of these clades were small vermiform paracoelomates that likely lacked indirect-developing planktotrophic larvae. Thus, the evolution of planktotrophic larvae may have been independently achieved at least three times within Bilateria. The nonmoulting clades evolved larvae that swim and feed via ciliated tufts and bands, presumably intercalating these forms within their early developmental systems. Within Ecdysozoa, feeding larvae lacked ciliary feeding tracts and evolved by modification of early instars, employing limbs or setae to generate feeding currents. The setting aside during larval life of cells that give rise to adult features is probably an adaptation associated with metamorphosis.     

Larval development in Cnidaria: A connection to bilateria?

Among the basal animal phyla, the Cnidaria display many characteristics similar to the Bilateria (the higher Metazoa). However, the relation of that outgroup phyla to the Bilateria is still equivocal. Additionally to morphological and genetic data, studies on cnidarian embryogenesis are essential to clarify the Cnidaria-Bilateria relationship. We analyzed cellular differentiation during planula larvae development of the jellyfish Podocoryne carnea. Within 24 to 30 h postfertilization, the diploblastic body structure and all cell types found in polyps have already differentiated in the larva. Whereas the differentiating smooth muscles, RFamide-positive nerve cells, or nematocytes (stinging cells) express no axial polarity, a newly discovered tyrosine-tubulin-positive nervous system develops gradually in repetitive patterns from anterior to posterior. These data demonstrate that part of the cnidarian nervous system develops from anterior to posterior in serially repeated patterns. This developmental mechanism seems to follow the bilaterian pattern and would have antedated the Cambrian explosion.     

Branching archaeocyaths as ecosystem engineers during the Cambrian radiation

The rapid origination and diversification of major animal body plans during the early Cambrian coincide with the rise of Earth's first animal-built framework reefs. Given the importance of scleractinian coral reefs as ecological facilitators in modern oceans, we investigate the impact of archaeocyathan (Class Archaeocyatha) reefs as engineered ecosystems during the Cambrian radiation. In this study, we present the first high-resolution, three-dimensional (3D) reconstructions of branching archaeocyathide (Order Archaeocyathida) individuals from three localities on the Laurentian paleocontinent. Because branched forms in sponges and corals display phenotypic plasticity that preserve the characteristics of the surrounding growth environment, we compare morphological measurements from our fossil specimens to those of modern corals to infer the surface conditions of Earth's first reefs. These data demonstrate that archaeocyaths could withstand and influence the flow of water, accommodate photosymbionts, and build topographically complex and stable structures much like corals today. We also recognize a stepwise increase in the roughness of reef environments in the lower Cambrian, which would have laid a foundation for more abundant and diverse coevolving fauna.     

寒武纪大爆发———早期后生动物辐射之谜:序言*

<正>随着中国经济的持续、稳定发展和国家政府对基础研究的日趋重视,我国科技投入力度正在逐年加大,包括古生物学在内的地球科学基础研究近十年来取得长足的进步和发展。近些年,我国的古生物学已开始在多门类起源、系统演化和环境背景研究中处于国际领先,在部分研究方向开始发挥重要国际引领作用。加之华南、华北保存的化石材料优势和若干国家重大项目的稳定、持续支持(Zhu et al.,2016a;Zhu and Li,2017),使我国在科研队伍、     

Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa

Organismal modifications to their physical and chemical environment play a significant role in structuring many modern ecosystems, and experimental evidence suggests that such behavior can increase diversity. Despite the important role such activities play in connecting ecology and evolution, less is known of the macroevolutionary impact of such influences, especially their role during major evolutionary transitions. The Ediacaran-Cambrian diversification of Metazoa encompassed the appearance and early diversification of virtually all major clades of marine animals and the establishment of metazoan-dominated ecosystems. Here we assess the role of positive ecological feedbacks using a new compilation of the first occurrences of all metazoan phyla, classes; orders and equivalent stem taxa, as well as data from a previously published compendium on fossils from the early to middle Cambrian of China. The results reveal relatively minor feedback during the Ediacaran, but a substantial increase during the Cambrian, principally through bioturbation and the appearance of a number of structural engineers, including sponges. Chemical modification of the environment through filtering and bioturbation seems to have had the largest impact. Data on taxic diversity is a poor proxy for abundance, or for the actual environmental impact of these activities, however. Future assessments of the influence of ecological feedbacks on this event will require standardized assessments of the abundance of taxa with different ecological roles.