Origin and evolution of animal life cycles

The ‘origin of larvae’ has been widely discussed over the years, almost invariably with the tacit understanding that larvae are secondary specializations of early stages in a holobenthic life cycle. Considerations of the origin and early radiation of the metazoan phyla have led to the conclusion that the ancestral animal (= metazoan) was a holopelagic organism, and that pelago-benthic life cycles evolved when adult stages of holopelagic ancestors became benthic, thereby changing their life style, including their feeding biology. The literature on the larval development and phylogeny of animal phyla is reviewed in an attempt to infer the ancestral life cycles of the major animal groups. The quite detailed understanding of larval evolution in some echinoderms indicates that ciliary filter-feeding was ancestral within the phylum, and that planktotrophy has been lost in many clades. Similarly, recent studies of the developmental biology of ascidians have demonstrated that a larval structure, such as the tail of the tadpole larva, can easily be lost, viz. through a change in only one gene. Conversely, the evolution of complex structures, such as the ciliary bands of trochophore larvae, must involve numerous genes and numerous adaptations. The following steps of early metazoan evolution have been inferred from the review. The holopelagic ancestor, blastaea, probably consisted mainly of choanocytes, which were the feeding organs of the organism. Sponges may have evolved when blastaea-like organisms settled and became reorganized with the choanocytes in collar chambers. The eumetazoan ancestor was probably the gastraea, as suggested previously by Haeckel. It was holopelagic and digestion of captured particles took place in the archenteron. Cnidarians and ctenophores are living representatives of this type of organization. The cnidarians have become pelago-benthic with the addition of a sessile, adult polyp stage; the pelagic gastraea-like planula larva is retained in almost all major groups, but only anthozoans have feeding larvae. Within the Bilateria, two major lines of evolution can be recognized: Protostomia and Deuterostomia. In protostomes, trochophores or similar types are found in most spiralian phyla; trochophore-like ciliary bands are found in some rotifers, whereas all other aschelminths lack ciliated larvae. It seems probable that the trochophore was the larval type of the ancestral, pelago-benthic spiralian and possible that it was ancestral in all protostomes. Most of the non-chordate deuterostome phyla have ciliary filter-feeding larvae of the dipleurula type, and this strongly indicates that the ancestral deuterostome had this type of larva.     

Choanoflagellates, choanocytes, and animal multicellularity

Abstract. It is widely accepted that multicellular animals (metazoans) constitute a monophyletic unit, deriving from ancestral choanoflagellate‐like protists that gave rise to simple choanocyte‐bearing metazoans. However, a re‐assessment of molecular and histological evidence on choanoflagellates, sponge choanocytes, and other metazoan cells reveals that the status of choanocytes as a fundamental cell type in metazoan evolution is unrealistic. Rather, choanocytes are specialized cells that develop from non‐collared ciliated cells during sponge embryogenesis. Although choanocytes of adult sponges have no obvious homologue among metazoans, larval cells transdifferentiating into choanocytes at metamorphosis do have such homologues. The evidence reviewed here also indicates that sponge larvae are architecturally closer than adult sponges to the remaining metazoans. This may mean that the basic multicellular organismal architecture from which diploblasts evolved, that is, the putative planktonic archimetazoan, was more similar to a modern poriferan larva lacking choanocytes than to an adult sponge. Alternatively, it may mean that other metazoans evolved from a neotenous larva of ancient sponges. Indeed, the Porifera possess some features of intriguing evolutionary significance: (1) widespread occurrence of internal fertilization and a notable diversity of gastrulation modes, (2) dispersal through architecturally complex lecithotrophic larvae, in which an ephemeral archenteron (in dispherula larvae) and multiciliated and syncytial cells (in trichimella larvae) occur, (3) acquisition of direct development by some groups, and (4) replacement of choanocyte‐based filter‐feeding by carnivory in some sponges. Together, these features strongly suggest that the Porifera may have a longer and more complicated evolutionary history than traditionally assumed, and also that the simple anatomy of modern adult sponges may have resulted from a secondary simplification. This makes the idea of a neotenous evolution less likely than that of a larva‐like choanocyte‐lacking archimetazoan. From this perspective, the view that choanoflagellates may be simplified sponge‐derived metazoans, rather than protists, emerges as a viable alternative hypothesis. This idea neither conflicts with the available evidence nor can be disproved by it, and must be specifically re‐examined by further approaches combining morphological and molecular information. Interestingly, several microbial lin°Cages lacking choanocyte‐like morphology, such as Corallochytrea, Cristidiscoidea, Ministeriida, and Mesomycetozoea, have recently been placed at the boundary between fungi and animals, becoming a promising source of information in addition to the choanoflagellates in the search for the unicellular origin of animal multicellularity.     

Diversification of the Metazoa: Ediacarans,colonies, and the origin of eumetazoan complexity by nested modularity

The Ediacaran biota is profoundly mysterious. There is a growing realization that these organisms should not be grouped in a single taxon, such as Petalonamae or Vendobionta, but debate continues on what the group as a whole represents. It is argued here that the Ediacarans constitute a broad, megascopic, paraphyletic grade of organization which overlaps the stem groups (and perhaps some crown groups) of the Porifera, Ctenophora, Cnidaria and Bilateria.

The modular organization of many Ediacarans suggests that they were fundamentally colonial organisms. The early disc‐shaped forms may have been solitary individuals, perhaps with a choanoflagellate or simple sponge‐like grade of organization; the modular forms may represent bud colonies of those entities. The more complex fronds, as well as other segmented and bilaterally symmetrical Ediacarans, seem to exhibit a trend toward higher levels of integration and individuation. This trend is comparable to those observed among more recent colonial organisms. Interpretation of modular Ediacarans as colonial organisms leads to a new perspective on the evolution of metazoans. It suggests that the earliest solitary Ediacarans furnished a framework for the development of cell and tissue specialization, including the formation of epithelia and complex connective tissues. Later colonial forms provided a mechanism to increase nested or hierarchical complexity, through duplication, integration, and individuation. Early acquisition of complexity had a profound impact on the subsequent evolution of metazoan body plans.

The Ediacarans seem to have evolved the range of colonial forms required to give rise to the radiation of complex bilaterians in the Cambrian. If this is true, it obviates the need to postulate the existence of the microscopic, acoelomate ancestors of basal metazoan taxa that are required by prevailing hypotheses bearing on the early evolution of the Metazoa.     

The contrariwise life of a parasitic, pedomorphic copepod with a non-feeding adult: ontogenesis, ecology, and evolution

Abstract. The extraordinary parasitic metanauplius larva of Caribeopsyllus amphiodiae is sexually dimorphic, with conspicuous gonads, and elaborate lens-bearing eyes. The parasites usually occur singly within their host, and grow for ≤5 months within the stomach of burrowing ophiuroids ( Amphiodia urtica ). They transform into free-living, semelparous, non-feeding adults that live only 2 weeks. The species' life-history pattern, with a larval period ∼10 × longer than the adult life span, is contrariwise to that of other copepods but not for animals with non-feeding adults of both sexes. It appears that the life cycle of C. amphiodiae is pedomorphic, and probably evolved through a delay of metamorphosis regulated by developmental hormones. We attribute the dominance of the larval phase to the greater potential for survival and growth of the enterozoic parasitic stages than of the free-living, post-metamorphic stages. We note that among marine invertebrates, non-feeding adults of both sexes occur exclusively in taxa with a complex life cycle, and that non-feeding adults of both sexes are never found in taxa that have small larvae and delayed maturation. They occur only when there is a large larva that can provide the adult stage with sufficient nutrient reserves for reproduction.     

Larval Planktotrophy—A Primitive Trait in the Bilateria?

The concept of Gösta Jägersten of a primary biphasic metazoan life-cycle, consisting of a planktotrophic larva and a benthic adult, forms the basis for several theories on metazoan phylogeny. In this paper the assumed planktotrophic life-style of the larva is critically analyzed and reconsidered. It is shown, in particular for the Mollusca, that a biphasic life-cycle with a lecithotrophic larva is probably the plesiomorphic condition. Character distribution and structural data suggest a parallel evolution of the downstream collecting system used in planktotrophic larvae or filter-feeding adults of gastropods, bivalves and other spiralian or aschelminth taxa. In the basic metazoans (Parazoa, Placozoa, coelenterates) direct or lecithotrophic development dominates by far. For the acoelomate (Platyhelminthes, Gnathostomulida) and pseudocoelomate taxa direct development is probably the plesiomorphic condition. The structural similarities of the upstream collecting system in tentaculate and deuterostome phyla may also be explained by parallel events of heterochrony out of an ancestor with adult filter-feeding. The main conclusion of this survey is that larval planktotrophy is likely to be secondary and not a plesiomorphic condition among the Bilateria. Accordingly, theories which are based on the assumed plesiomorphy of larval planktotrophy of the Bilateria, need careful reevaluation.     

Six major steps in animal evolution: are we derived sponge larvae?

A review of the old and new literature on animal morphology/embryology and molecular studies has led me to the following scenario for the early evolution of the metazoans. The metazoan ancestor, "choanoblastaea," was a pelagic sphere consisting of choanocytes. The evolution of multicellularity enabled division of labor between cells, and an "advanced choanoblastaea" consisted of choanocytes and nonfeeding cells. Polarity became established, and an adult, sessile stage developed. Choanocytes of the upper side became arranged in a groove with the cilia pumping water along the groove. Cells overarched the groove so that a choanocyte chamber was formed, establishing the body plan of an adult sponge; the pelagic larval stage was retained but became lecithotrophic. The sponges radiated into monophyletic Silicea, Calcarea, and Homoscleromorpha. Homoscleromorph larvae show cell layers resembling true, sealed epithelia. A homoscleromorph-like larva developed an archenteron, and the sealed epithelium made extracellular digestion possible in this isolated space. This larva became sexually mature, and the adult sponge-stage was abandoned in an extreme progenesis. This eumetazoan ancestor, "gastraea," corresponds to Haeckel's gastraea. Trichoplax represents this stage, but with the blastopore spread out so that the endoderm has become the underside of the creeping animal. Another lineage developed a nervous system; this "neurogastraea" is the ancestor of the Neuralia. Cnidarians have retained this organization, whereas the Triploblastica (Ctenophora+Bilateria), have developed the mesoderm. The bilaterians developed bilaterality in a primitive form in the Acoelomorpha and in an advanced form with tubular gut and long Hox cluster in the Eubilateria (Protostomia+Deuterostomia). It is indicated that the major evolutionary steps are the result of suites of existing genes becoming co-opted into new networks that specify new structures. The evolution of the eumetazoan ancestor from a progenetic homoscleromorph larva implies that we, as well as all the other eumetazoans, are derived sponge larvae.     

An evolutionary history of the FGF superfamily

Fibroblast growth factors (FGF) are associated with multiple developmental and metabolic processes in triploblasts, and perhaps also in diploblasts. The evolution of the FGF superfamily has accompanied the major morphological and functional innovations of metazoan species. The study of FGFs throughout species shows that the FGF superfamily can be subdivided in eight families in present-day organisms and has evolved through phases of gene duplications and gene losses. At least two major expansions of the superfamily can be recognized: a first expansion increased the number of FGFs from one or few archeo-FGFs to eight proto-FGFs, prototypic of the eight families. A second expansion, which took place during euchordate evolution, is associated with genome duplications. It increased the number of members in the families. Subsequent losses reduced that number to the present-day figures.     

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.     

Homology of ciliary bands in Spiralian Trochophores

A number of hypotheses have been presented regarding the originsof the metazoans and, more specifically, the Bilateria. Usingvarious phylogenetic analyses, characteristics have been mappedon phylogenetic trees to infer ancestral body plans and lifehistory strategies of those ancestors. Many arguments on theevolution of the Bilateria are based on the presumed homologyof certain characteristics of extant larva and adults, includingvarious ciliated bands involved in feeding and locomotion. Thisarticle considers a recent study indicating that the second,downstream-collecting, ciliated band in the veliger larva ofthe gastropod mollusc, Crepidula fornicata, is actually derivedfrom secondary trochoblasts (derived from second quartet micromeres),that normally form part of the prototrochal band found in otherspiralian phyla (Hejnol et al. 2007). Despite previous arguments,these new findings suggest that the second ciliated band inthe veliger larva is not homologous to the metatroch found inthe trochophore larva of some other spiralians, such as theannelid, Polygordius lacteus. In the latter case, the metatrochwas reported to be formed by a different set of lineage precursors(derived from third quartet micromeres) (Woltereck 1904). Thesefindings have important implications for the interpretationof various hypotheses related to the evolution of metazoan phyla.     

The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it?

The biphasic (pelagobenthic) life cycle is found throughoutthe animal kingdom, and includes gametogenesis, embryogenesis,and metamorphosis. From a tangled web of hypotheses on the originand evolution of the metazoan pelagobenthic life cycle, currentopinion appears to favor a simple, larval-like holopelagic ancestorthat independently settled multiple times to incorporate a benthicphase into the life cycle. This hypothesis derives originallyfrom Haeckel's (1874) Gastraea theory of ontogeny recapitulatingphylogeny, in which the gastrula is viewed as the recapitulationof a gastraean ancestor that evolved via selection on a simple,planktonic hollow ball of cells to develop the capacity to feed.Here, we propose an equally plausible hypothesis that the originof the metazoan pelagobenthic life cycle was a direct consequenceof sexual reproduction in a likely holobenthic ancestor. Indoing so, we take into account new insights from poriferan developmentand from molecular phylogenies. In this scenario, the gastruladoes not represent a recapitulation, but simply an embryologicalstage that is an outcome of sexual reproduction. The embryocan itself be considered as the precursor to a biphasic lifestyle,with the embryo representing one phase and the adult anotherphase. This hypothesis is more parsimonious because it precludesthe need for multiple, independent origins of the benthic form.It is then reasonable to consider that multilayered, ciliatedembryos ultimately released into the water column are subjectto natural selection for dispersal/longevity/feeding that setsthem on the evolutionary trajectory towards the crown metazoanplanktonic larvae. These new insights from poriferan developmentthus clearly support the intercalation hypothesis of bilaterianlarval evolution, which we now believe should be extended todiscussions of the origin of biphasy in the metazoan last commonancestor.     

EVOLUTIONARY LOSS OF LARVAL FEEDING: DEVELOPMENT,FORM AND FUNCTION IN A FACULTATIVELY FEEDING LARVA,BRISASTER LATIFRONS

Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.     

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.     

The origin of Metazoa: a transition from temporal to spatial cell differentiation

For over a century, Haeckel's Gastraea theory remained a dominant theory to explain the origin of multicellular animals. According to this theory, the animal ancestor was a blastula‐like colony of uniform cells that gradually evolved cell differentiation. Today, however, genes that typically control metazoan development, cell differentiation, cell‐to‐cell adhesion, and cell‐to‐matrix adhesion are found in various unicellular relatives of the Metazoa, which suggests the origin of the genetic programs of cell differentiation and adhesion in the root of the Opisthokonta. Multicellular stages occurring in the complex life cycles of opisthokont protists (mesomycetozoeans and choanoflagellates) never resemble a blastula. Here, we discuss a more realistic scenario of transition to multicellularity through integration of pre‐existing transient cell types into the body of an early metazoon, which possessed a complex life cycle with a differentiated sedentary filter‐feeding trophic stage and a non‐feeding blastula‐like larva, the synzoospore. Choanoflagellates are considered as forms with secondarily simplified life cycles.     

EVOLUTION OF GREGARIOUSNESS IN APOSEMATIC BUTTERFLY LARVAE: A PHYLOGENETIC ANALYSIS

Gregariousness ought to be disadvantageous for palatable organisms that live exposed and are relatively immobile and small in comparison to potential predators. Therefore, the idea that unpalatability generally evolves before egg clustering/larval gregariousness in butterflies was tested. Aposematic coloration in the larva was used as the criterion of unpalatability (it is argued that Batesian mimicry is rare in butterfly larvae), and the relative order of evolution of aposematism and gregariousness was inferred through phylogenetic analysis. Here, existing phylogenies were used, and the analysis was based on an assumption of a minimum number of evolutionary changes (parsimony). A total of 23 cases of independent evolution of gregariousness and 12 cases of independent evolution of aposematic coloration were found. In five cases, gregariousness evolved in cryptic species, the palatability of which is unknown. For lineages in which both unpalatability, as evidenced by aposematic coloration, and gregariousness were found and the two evolutionary events could be separated, unpalatability always preceded gregariousness: five cases of independent evolution of warning coloration were followed by a total of 15 cases of independent evolution of gregariousness. In no lineage did gregariousness evolve before warning coloration. It is thus concluded that unpalatability is an important predisposing factor for the evolution of egg clustering and larval gregariousness in butterflies. Insofar as kin selection is related to larval gregariousness, this study indicates that kin selection is of minor importance for the evolution of both unpalatability and warning coloration.     

Effects of age and liquid holding on the UV-radiation sensitivities of wild-type and mutant Caenorhabditis elegans dauer larvae

The dauer larva is a facultative developmental stage in the life cycle of the nematode Caenorhabditis elegans. Dauer larvae, which can survive under starvation for over 60 days, resume normal development when feeding is resumed. Wild-type (N2) and 4 radiation-sensitive (rad) mutant dauer larvae were tested for their abilities to develop into adults after UV-irradiation. The rad-3 mutant was over 30 times as sensitive as N2; rad-1, rad-2 and rad-7 mutants were not hypersensitive. Irradiation also delayed development in survivors. Wild-type dauer larvae did not differ in radiation sensitivity from 0 through 50 days of age. There was no liquid holding recovery (LHR); that is, survival did not increase when wild-type dauer larvae were held in buffer after irradiation.     

条背萤幼虫水生适应性形态与游泳行为研究

研究了条背萤Luciolasubstriata幼虫的形态特征及其对游泳行为的适应。形态及扫描电镜观察发现,条背萤幼虫存在二态现象。1～2龄幼虫虫体扁平,多毛。有7对呼吸鳃,分别位于腹部第1～7节。3～6龄幼虫虫体扁平呈船形,无呼吸鳃,靠气管呼吸。二者均具有扁平桨状的足、燕尾状尾节及位于尾节末端的圆柱形粘附器官。条背萤幼虫游动时身体腹面朝上,呈仰泳姿态,足向后划水。3～6龄幼虫仰泳时足共有8种摆动姿势。幼虫仰泳时足摆动1个周期所需时间为(0.611±0.16)s。腹部末端可上下左右摆动,当幼虫向前游动时,尾部上下摆动1个周期所需时间为(1.795±0.44)s。幼虫的游泳速度为(0.85±0.16)mh。仰泳中的幼虫改变方向时,头部和尾部同时向身体的一侧弯曲,当头部与尾部呈近90°时,幼虫用力将尾部伸直,此时水产生一个反作用力继续推动幼虫转向,幼虫转向的范围为0～90°。条背萤2种类型幼虫呼吸系统的不同决定着幼虫外部形态的差异及游泳行为的不同,而导致这种呼吸系统、形态及运动行为不同的原因很可能是条背萤对环境的适应性进化。     

Evasion of phagotrophic predation by protist hosts and innate immunity of metazoan hosts by Legionella pneumophila

Legionella pneumophila is a ubiquitous environmental bacterium that has evolved to infect and proliferate within amoebae and other protists. It is thought that accidental inhalation of contaminated water particles by humans is what has enabled this pathogen to proliferate within alveolar macrophages and cause pneumonia. However, the highly evolved macrophages are equipped with more sophisticated innate defence mechanisms than are protists, such as the evolution of phagotrophic feeding into phagocytosis with more evolved innate defence processes. Not surprisingly, the majority of proteins involved in phagosome biogenesis (~80%) have origins in the phagotrophy stage of evolution. There are a plethora of highly evolved cellular and innate metazoan processes, not represented in protist biology, that are modulated by L. pneumophila, including TLR2 signalling, NF‐κB, apoptotic and inflammatory processes, histone modification, caspases, and the NLRC–Naip5 inflammasomes. Importantly, L. pneumophila infects haemocytes of the invertebrate Galleria mellonella, kill G. mellonella larvae, and proliferate in and kill Drosophila adult flies and Caenorhabditis elegans. Although coevolution with protist hosts has provided a substantial blueprint for L. pneumophila to infect macrophages, we discuss the further evolutionary aspects of coevolution of L. pneumophila and its adaptation to modulate various highly evolved innate metazoan processes prior to becoming a human pathogen.     

Development of the nervous system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals both deuterostome- and trochozoan-like features

Background

Inferences concerning the evolution of invertebrate nervous systems are often hampered by the lack of a solid data base for little known but phylogenetically crucial taxa. In order to contribute to the discussion concerning the ancestral neural pattern of the Lophotrochozoa (a major clade that includes a number of phyla that exhibit a ciliated larva in their life cycle), we investigated neurogenesis in Phoronopsis harmeri, a member of the poorly studied Phoronida, by using antibody staining against serotonin and FMRFamide in combination with confocal microscopy and 3D reconstruction software.

Results

The larva of Phoronopsis harmeri exhibits a highly complex nervous system, including an apical organ that consists of four different neural cell types, such as numerous serotonin-like immunoreactive flask-shaped cells. In addition, serotonin- and FMRFamide-like immunoreactive bi- or multipolar perikarya that give rise to a tentacular neurite bundle which innervates the postoral ciliated band are found. The preoral ciliated band is innervated by marginal serotonin-like as well as FMRFamide-like immunoreactive neurite bundles. The telotroch is innervated by two neurite bundles. The oral field is the most densely innervated area and contains ventral and ventro-lateral neurite bundles as well as several groups of perikarya. The digestive system is innervated by both serotonin- and FMRFamide-like immunoreactive neurites and perikarya. Importantly, older larvae of P. harmeri show a paired ventral neurite bundle with serial commissures and perikarya.

Conclusions

Serotonin-like flask-shaped cells such as the ones described herein for Phoronopsis harmeri are found in the majority of lophotrochozoan larvae and therefore most likely belong to the ground pattern of the last common lophotrochozoan ancestor. The finding of a transitory paired ventral neurite bundle with serially repeated commissures that disappears during metamorphosis suggests that such a structure was part of the ??ur-phoronid?? nervous system, but was lost in the adult stage, probably due to its acquired sessile benthic lifestyle.