The coelom and the origin of the annelid body plan

The biphasic life cycle in annelids is characterized by two completely different types of organisation, i.e. the acoelomate/pseudocoelomate larva and the coelomate adult. Based on this observation the recent literature on the different assumptions on the organisation of the bilaterian stem species with special emphasis on the evolution of the annelid body plan is reviewed. The structure of the coelomic lining ranges between a simple myoepithelium composed of epithelio-muscle cells and a non-muscular peritoneum that covers the body wall muscles. The direction of the evolution of these linings is discussed with respect to coelomogenesis. As the coelom originates from mesodermal cell bands, different assumption on the acoelomate condition in Bilateria can be substantiated. The origin of segmentation in annelids is explained by current hypothesis. Although no final decision can be made concerning the origin of the annelid body plan and the organisation of the bilaterian stem species, this paper elaborates those questions that need to be resolved to unravel the relation between the different body plans.     

Structure and development of nephridia in Annelida and related taxa

Two different kinds of filtration nephridia, protonephridia and metanephridia, are described in Polychaeta. During ontogenesis protonephridia generally precede metanephridia. While the latter are segmentally arranged, protonephridia are characteristic for the larva and are the first nephridial structure formed during ontogenesis. There is strong evidence that both organs depend on the same information and that their specific structure depends on the way in which the coelom is formed and which final expansion it gains. While metanephridia are regarded to be homologous throughout the polychaetes, protonephridia seem to have evolved in several lineages. Some of the protonephridia closely resemble less differentiated stages of metanephridial development, so that protonephridial evolution can be explained by truncation of the metanephridial development. Nevertheless, structural details are large enough to allow us to expect information on the polychaete evolution if the database on polychaete nephridia increases. A comparison of the polychaete metanephridia with those of the Clitellata and Sipuncula reveals some surprising details. In Clitellata the structure of the funnel is quite uniform in microdrilid oligochaetous Clitellata and resembles that of the aeolosomatids. Like the nephridia in the polychaete taxa Sabellida and Terebellida, those of the Sipunucla possess podocytes covering the coelomic side of the duct.     

Structure and development of the nephridia of Tomopteris helgolandica (Annelida)

 Nephridial diversity is high in Phyllodocida (Annelida) and ranges from protonephridia to metanephridia. The nephridia of Tomopteris helgolandica (Tomopteridae) can be characterized as metanephridia which bear a multiciliated solenocyte. This cell is medially apposed to the proximal part of the nephridial duct and bears several cilia, each of which is surrounded by a ring of 13 microvilli. An extracellular matrix connects the microvilli and thus leads to the impression of a tube surrounding the central cilium. Each tube separately enters a subjacent duct cell and the cilia extend into a cup-shaped compartment within the duct cell. This compartment is not connected to the duct. The funnel consists of eight multiciliated cells and is connected to the nephridial duct, which initially runs intercellularly and later percellularly. The last duct cell bears a neck-like process which pierces the subepidermal basal membrane and is connected to epidermal cells forming a small invagination, the nephropore. The nephridia of T. helgolandica develop from a band of cells and all structural components are differentiated at an early developmental stage. Further development is characterized by enlargment of the funnel, ciliogenesis in the solenocyte, merging of different sections of the duct and, finally, the formation of the nephropore. An evaluation of the nephridia of T. helgolandica leads to the hypothesis that the nephridial diversity in Phyllodocida can be explained by the retainment of different stages in the transition of protonephridia into metanephridia; this is caused by the formation of a ciliated funnel at different ontogenetic stages. Although the protonephridia in Phyllodocida are regarded as primary nephridial organs, protonephridia are also presumed to have evolved secondarily in progenetic interstitial species of the Annelida by an incomplete differentiation of the nephridial anlage. Accepted: 18 December 1996     

Ultrastructure and significance of the transitory nephridia in Erpobdella octoculata (Hirudinea, Annelida)

In early developmental stages of Erpobdella octoculata two pairs of transitory nephridia occur which degenerate during the formation of the body segments. Because in the ground pattern of Annelida the first nephridia formed during ontogenesis are protonephridia, it can be assumed that the transitory nephridia of E. octoculata are homologous to the larval protonephridia (head kidneys) of Polychaeta. To test this hypothesis two cryptolarvae of E. octoculata were investigated ultrastructurally. Both pairs of transitory nephridia are serially arranged to either side of the midgut vestigium. Each organ consists of a coiled duct that opens separately to the exterior by an intraepidermal nephridiopore cell. The duct is percellular and formed by seventeen cells. Adluminal adherens and septate junctions connect all duct cells; the most proximal duct cell completely encloses the terminal end of the duct lumen. A filtration structure characteristic for protonephridia is lacking. Additionally, the entire organ lacks an inner ciliation. Morphologically and ultrastructurally the transitory nephridia of E. octoculata show far reaching congruencies with the segmental metanephridia in different species of the Hirudinea. These congruencies support the assumption that formation of transitory nephridia and definitive metanephridia in Hirudinea depends on the same genetic information. The same inherited information is assumed to cause the development of larval head kidneys and subsequently formed nephridia in different species of the Polychaeta. Thus, the presumed identical fate of a segmentally repeated nephridial anlage supports the hypothesis of a homology between the transitory nephridia in Hirudinea species and the protonephridial head kidneys in the ground pattern of the Polychaeta. We, therefore, assume that functional constraints lead to a modification of the protonephridial head kidneys in Hirudinea and explain ultrastructural differences between the transitory nephridia in Hirudinea and the protonephridia in Polychaeta. Accepted: 11 December 2000     

Ultrastructure and development of the nephridia in Anaitides mucosa (Annelida,Polychaeta)

Different developmental stages (trochophores, nectochaetae, non-mature and mature adults) of Anaitides mucosa were investigated ultrastructurally. A. mucosa has protonephridia throughout its life; during maturity a ciliated funnel is attached to these organs. The protonephridial duct cells are multiciliated, while the terminal cells are monociliated. The single cilium is surrounded by 14 microvilli which extend into the duct lumen without coming into any contact with the duct cells. Corresponding ultrastructure and development indicate that larval and adult protonephridia are identical in A. mucosa. Differences between various developmental stages can be observed only in the number of cells per protonephridium. A comparison between the funnel cells, the cells of the coelothel and the duct cells reveals that the ciliated funnel is a derivative of the duct. Due to the identical nature of the larval and postlarval protonephridia, such a funnel cannot be a secondary structure. In comparison with the mesodermally derived metanephridial funnel in phoronids it seems likely that the metanephridia of annelids and phoronids evolved convergently.     

Ultrastructure and relationship between protonephridia and metanephridia in Phoronis muelleri (Phoronida)

Summary The actinotrocha of Phoronis muelleri has one pair of ectodermally derived, monociliated protonephridia. The duct runs mainly between the epidermis and the lining of the hyposphere coelom, pierces the septum and extends into the blastocoel. The proximal part is branched and closed up by terminal complexes consisting of two morphologically different cells which both serve filtration. During metamorphosis, the terminal complexes and the branches of the duct are cast off. The cells degenerate, pass into the remaining duct and are endocytosed by the duct cells. After metamorphosis the remaining part of the protonephridial duct is U-shaped, blindly closed and borders on the prospective lophophoral vessel. In a later stage the duct receives a ciliated funnel, which consists of monociliated epithelio-muscle cells and is a derivative of the lining of the metacoel. Thus, a part of the protonephridial duct of the larva and the whole metanephridial duct of the adult are identical. Aspects of a possible homology between phoronid nephridia and such organs in other bilaterians are discussed.     

The larval nephridia of the brackish-water polychaete,Nereis diversicolor

The larval nephridia of the brackish-water polychaete Nereis diversicolor are described for the first time, and have been studied to determine if their times of development and structural characteristics are consistent with a role in the osmotic regulation of the larva. As shown in serial paraffin sections and by interference-contrast optics, the nephridia of the three-setiger larva consist of a single pair of very large metanephridia, arising in the 3rd larval setiger, but with their elongated terminal ducts and coiled ciliated tubules pushed forward into the 2nd setiger; their open metanephrostomes and anterior anchoring filaments lie dorsal to the 2nd set of setae. In contrast, the definitive or juvenile metanephridia, arising in the 4th and subsequently formed setigerous segments, have short terminal ducts and coiled ciliated tubules confined to the segments on which their external nephropores open; their nephrostomes are ventrally located and open into the rear of the next anterior segment. These findings are in contrast to the claims of Edouard Meyer (1887), who described two pairs of closed protonephridia in the 2nd and 3rd larval setigers of Perinereis cultrifera. Although it is not excluded that the single larval pair of metanephridia of N. diversicolor may arise as protonephridia, Meyer's claim of two pairs of larval protonephridia was an observational error. The larval nephridia of the marine Platynereis dumerilii resemble in form, but are considerably smaller than, those of N. diversicolor. It is concluded that the hypertrophied pair of larval metanephridia of N. diversicolor is an evolutionary adaptation to existence in habitats of low and unpredictably varying salinity. Their development occurs irrespective of the prevailing salinity; hence, it must be genetically determined.     

Back in time: a new systematic proposal for the Bilateria

Conventional wisdom suggests that bilateral organisms arose from ancestors that were radially, rather than bilaterally, symmetrical and, therefore, had a single body axis and no mesoderm. The two main hypotheses on how this transformation took place consider either a simple organism akin to the planula larva of extant cnidarians or the acoel Platyhelminthes (planuloid-acoeloid theory), or a rather complex organism bearing several or most features of advanced coelomate bilaterians (archicoelomate theory). We report phylogenetic analyses of bilaterian metazoans using quantitative (ribosomal, nuclear and expressed sequence tag sequences) and qualitative (HOX cluster genes and microRNA sets) markers. The phylogenetic trees obtained corroborate the position of acoel and nemertodermatid flatworms as the earliest branching extant members of the Bilateria. Moreover, some acoelomate and pseudocoelomate clades appear as early branching lophotrochozoans and deuterostomes. These results strengthen the view that stem bilaterians were small, acoelomate/pseudocoelomate, benthic organisms derived from planuloid-like organisms. Because morphological and recent gene expression data suggest that cnidarians are actually bilateral, the origin of the last common bilaterian ancestor has to be put back in time earlier than the cnidarian-bilaterian split in the form of a planuloid animal. A new systematic scheme for the Bilateria that includes the Cnidaria is suggested and its main implications discussed.     

The phylogenetic position of Brachiopoda—a comparison of morphological and molecular data

Analyses of rRNA and rDNA among Metazoa result in a hypothesis of a sistergroup relationship of Brachiopoda and certain spiralian taxa, whereas analyses of morphological data imply that Brachiopoda show affinities to Deuterostomia within the Radialia. Regarding Brachiopoda as a derived spiralian taxon must be followed by a reinterpretation of the evolution of distinct brachiopod morphological characters—like cleavage pattern, coelom or larva. The experimental insertion of a monophyletic taxon consisting of Brachiopoda and Phoronida into a widely accepted phylogenetic tree of Spiralia leads to the hypothesis that at least trimeric organization, mesosomal tentacular apparatus and heterogeneously assembled metanephridia are products of convergent evolution in Brachiopoda plus Phoronida and Deuterostomia. The hypothesis of a radialian nature of Brachiopoda and Phoronida, as implied by morphological data, remains as the most parsimonious possibility to explain the evolution of seven regarded characters (cleavage pattern, larva, tentacular apparatus, coelom, metameric segmentation, metanephridia and chaetae) in Brachiopoda. Due to the conflicting results of both methods a hitherto undetected systematical problem is discussed possibly hindering data comparability. If the course of evolution can principally be inferred from the information preserved in recent and fossil animals, the results should be congruent in the analyses of both, molecular and morphological data.     

Protonephridia in the larvae of the paleonemertean species Carinoma mutabilis (Carinomidae,Nemertea) and Cephalothrix (Procephalothrix) filiformis (Cephalothricidae,Nemertea)

During spiralian development, the first pair of nephridia forms anterior to the mouth. Each organ consists of a few cells, which is characteristic for spiralian larvae. In nemerteans, one of the unambiguously spiralian taxa, so far protonephridia, has been reported only in advanced pilidium larvae, where they likely persist as juvenile and adult nephridia. These organs have not been recorded in larvae of the basally branching nemertean taxa. In search for these organs, we examined the ultrastructure of pelagic planuliform larvae of the palaeonemerteans Carinoma mutabilis and Cephalothrix (Procephalothrix) filiformis. In both species, a pair of protonephridia is located at the level of the stomodaeum. Each protonephridium of C. mutabilis consists of two terminal cells, two duct cells and one nephropore cell, while that of C. filiformis consists of three terminal cells, three duct cells and one nephropore cell. In C. mutabilis and in C. filiformis, all terminal cells contribute to forming a compound filtration structure. In both species, the protonephridia seem to develop subepidermally, since in C. filiformis, the nephropore cells pierce the larval epidermis and in C. mutabilis, the nephropores are initially covered by the binucleated multiciliated trophoblast cells. On the fifth day, these cells degenerate, so that the protonephridium becomes functional. The occurrence of protonephridia in the larvae of both paleonemertean species is in accordance with the hypothesis that a common ancestor of Nemertea and Trochozoa had a larval stage with a pair of protonephridia. This does not contradict previous hypotheses on placing the Nemertea as an ingroup of the Trochozoa or Spiralia (= Lophotrochozoa). Whether these protonephridia are restricted to the larval phase or whether they are transformed into the adult protonephridia, like those of the pilidium larva, remains to be answered.     

Nachtrag zur “Wurmtheorie” der Vertebraten-Evolution1

This paper presents some new arguments for the metameric-wonn-theory for the evolution of the Vertebrates (Gutmann 1966a). Metameric coelomoducts in Enteropneust larvae (Goodrich 1947) which should be interpreted as metanephridia show that the Enteropneusts can be derived from metameric Chordate-like predecessors. The myomeres of Branchiostoma are no solid organs as there exist sclerocoels. These must be interpreted as vestigial coelomic cavities. They can be cited as a proof for the metameric worm-theory. They function as a canal system, which gathers excretory stuff in the myomeres which these organs could otherwise not get rid of. The coelom-cavities are cleaned by the protonephridia in the gill region. Some additional details of the phylogenetic transformation of metameric coelom cavities into myomeres are reconstructed. It is shown that the problem of coelomic and myomeric metamerism cannot be solved in the way proposed in the literature concerned with this question. The metameric-worm-theory for the evolution of the Vertebrates pretends that metameric metanephridia were fused on the lower level of Vertebrate phylogeny and formed the archinephric ducts. A paper of Goodrich (1947) shows that there are similar cases of fused metanephridia in some Annelids. These are parallels to the postulated formation of the metanephridia in the lowest Vertebrates. The archinephric duct acquired its muscular coat when it was formed by fusion of metanephridia in the bodywall. Muscles of the body wall took over a new function by making peristaltic movements of the newly formed archinephric ducts possible. When the archinephric duct was moved back into the coelom it did not lose the still functioning muscular coat.     

Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

ABSTRACT: BACKGROUND: Two types of excretory systems, protonephridia and metanephridial systems are common among bilaterians. The homology of protonephridia of lophotrochozoan taxa has been widely accepted. In contrast, the homology of metanephridial systems -- including coelomic cavities as functional units -- among taxa as well as the homology between the two excretory systems is a matter of ongoing discussion. This particularly concerns the molluscan kidneys, which are mostly regarded as being derived convergently to the metanephridia of e.g. annelids because of different ontogenetic origin. A reinvestigation of nephrogenesis in polyplacophorans, which carry many primitive traits within molluscs, could shed light on these questions. RESULTS: The metanephridial system of Lepidochitona corrugata develops rapidly in the early juvenile phase. It is formed from a coelomic anlage that soon achieves endothelial organization. The pericardium and heart are formed from the central portion of the anlage. The nephridial components are formed by outgrowth from lateral differentiations of the anlage. Simultaneously with formation of the heart, podocytes appear in the atrial wall of the pericardium. In addition, renopericardial ducts, kidneys and efferent nephroducts, all showing downstream ciliation towards the internal lumen, become differentiated (specimen length: 0.62 mm). Further development consists of elongation of the kidney and reinforcement of filtration and reabsorptive structures. CONCLUSIONS: During development and in fully formed condition the metanephridial system of Lepidochitona corrugata shares many detailed traits (cellular and overall organization) with the protonephridia of the same species. Accordingly, we suggest a serial homology of various cell types and between the two excretory systems and the organs as a whole. The formation of the metanephridial system varies significantly within Mollusca, thus the mode of formation cannot be used as a homology criterion. Because of similarities in overall organization, we conclude that the molluscan metanephridial system is homologous with that of the annelids not only at the cellular but also at the organ level.     

THE FUNCTIONAL ORGANIZATION OF FILTRATION NEPHRIDIA

(1) Based on the classical studies of Goodrich, protonephridia are believed to be phylogenetic antecedents of metanephridia. It is argued here that the primary factor determining the type of nephridium expressed is body size rather than phylogenetic status. (2) The proposed model defines a nephridium functionally and predicts two general configurations for filtration nephridia in animals. (3) Application of the model to metanephridial and protonephridial systems indicates differences in the sites of ultrafiltration and mechanisms of pressure generation. (4) Metanephridial systems function by muscle-mediated filtration of vascular fluid into a coelomic space before modification by an excretory duct. (5) Protonephridial systems function by cilia-mediated filtration of extracellular fluid into the lumen of a protonephridial terminal cell before modification in an adjoining duct. (6) The model predicts a correlation between animals with blood vessels and metanephridia, and animals without blood vessels and protonephridia. The correlation is shown to be nearly perfect. (7) Exceptions to the model are discussed. (8) Original experimental evidence is given for the permeability of the protonephridial terminal cell to iron dextran and its reabsorption by the protonephridial duct in the polychaete, Glycera dibranchiata. (9) Experimental data for proto- and metanephridial systems are summarized and shown to support the proposed model. (10) The ultrastructure of the exceptional amphioxus ‘protonephridium’ is reviewed and original data are presented. Its organization is structurally and perhaps functionally intermediate between proto- and metanephridial systems. (11) An original ultrastructural comparison is made of monociliated nitration cells in a size range of larval invertebrates from five phyla. Filtration cells that are structurally intermediate between protonephridial solenocytes and metanephridial podocytes are noted in larvae intermediate in body size between the two extremes. The comparative data suggest that (i) podocytes and solenocytes are homologous cells and (ii) that body size is correlated with which of the two designs is expressed. (12) The fates of larval podocytes are followed through metamorphosis in three species. The results confirm the equivalence of podocytes and solenocytes as suggested by the comparative analysis. They further indicate that which morph is expressed is a function of body design factors discussed in the model. (13) Protonephridia are believed to be primitive to metanephridia because they occur in presumably primitive animals and in ontogenetic stages of many animals with metanephridia as adults. It is suggested here that the distribution of protonephridia is related to small body size and the lack of blood vessels, regardless of phylogenetic status. The occurrence of protonephridia in the larvae of species with metanephridia as adults is explained similarly as a function of the small larval size and lack of blood vessels.     

Ultrastructure of the metanephridia of Terebratulina retusa and Crania anomala (Brachiopoda)

Adult specimens of Terebratulina retusa and Crania anomala have one pair of metanephridia. Each metanephridium is composed of a ciliated nephridial funnel (nephrostome) and an outleading nephridial canal, thus, these organs are open ducts connecting the metacoel of the animal with the outer medium. In both species, the inner side of a nephrostome is lined by a columnar monociliated epithelium which contacts the coelothel within one of the two ileoparietal bands. The coelothel contains basal filaments (in C. anomala these are definite myofilaments). The canal epithelium also consists of monociliated columnar cells which differ from the nephrostome epithelial cells in size and some cell components. Within the nephropore, the canal epithelium makes contact with the so-called inner mantle epithelium which lines the mantle cavity. The nephrostome epithelial cells and the canal epithelial cells never contain any contractile filaments. There are always continuous transitions between these different epithelia and distinct borders cannot be observed. The present results, especially in comparison to Phoronida, do not contradict the hypothesis of a coelothelially derived nephridial funnel and an ectodermal nephridial duct in Brachiopoda. But with regard to the differences between Phoronida and Brachiopoda (larval protonephridia and podocytes in the adults are unknown in Brachiopoda), further investigations have to be done to test the hypothesis of such heterogeneously assembled metanephridia.     

The nephridia of the interstitial polychaete Hesionides arenaria and their phylogenetic significance (Polychaeta,Hesionidae)

Summary The small hesionid polychaete Hesionides arenaria possesses paired segmental excretory organs that closely resemble solenocytic protonephridia. The nephridium consists of one terminal cell and four tubule cells which form the emission channel. From the terminal cell, up to six flagella arise each surrounded by a weir of ten regularly arranged cytoplasmic rods. The structure of the cytoplasm of three of the following cells suggests that they function in active transport and storage. Because all of the larger, more primitive species of this family are equipped with metanephridia, the possibility is discussed that these organs have been developed out of metanephridia. The Hesionides arenaria nephridium may be a morphological stage in the evolutionary pathway from metanephridia to solenocytes. This would mean that solenocytes can no longer be considered to be homologous in every case with other protonephridial organs in polychaetes and may well be derived several times independently out of metanephridia or true protonephridia.     

Development of the excretory system in the polyplacophoran mollusc,Lepidochitona corrugata: The protonephridium

A single pair of protonephridia is the typical larval excretory organ of molluscs. Their presence in postlarval developmental stages was discovered only recently. We found that the protonephridia of the polyplacophoran mollusc, Lepidochitona corrugata, achieve their most elaborate differentiation and become largest during the postlarval period. This study describes the protonephridia of L. corrugata using light and electron microscopy and interactive three‐dimensional visualization. We focus on the postlarval developmental period, in which the protonephridia consist of three parts: the terminal part with the ultrafiltration sites at the distal end, the voluminous protonephridial kidney, and the efferent nephroduct leading to the nephropore. The ultrafiltration sites show filtration slits between regularly arranged thin pedicles. The ciliary flame originates from both the terminal cell and the duct cells of the terminal portion. The efferent duct also shows ciliation. The most conspicuous structures, the protonephridial kidneys, are voluminous swellings composed of reabsorptive cells (“nephrocytes”). These cells exhibit strong vacuolization and an infolding system increasing the basal surface. The protonephridial kidneys, previously not reported at such a level of organization in molluscs, strikingly resemble (metanephridial) kidneys of adult molluscan excretory systems. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Review of data for a morphological look on Xenacoelomorpha (Bilateria incertae sedis)

Recent investigations by means of high-tech morphology, evo-devo studies and molecular data suggest that the taxon Xenacoelomorpha (Nemertodermatida and Acoela plus Xenoturbella), formerly considered as primitive flatworms (Plathelminthes) or even bivalve Mollusca, represents either a quite plesiomorphic grouping as the earliest bilaterian offshoot or but is a substantially reduced and simplified sidebranch of ambulacralian Deuterostomia. Herein, I provide a compilation and review of the current morphological data and possible interpretations of the various character states. Phenotypic and genotypic data suggest monophyly of Xenacoelomorpha. There is no specific similarity between xenacoelmorphs and deuerostome larvae, and reduction appears improbable in free-living and predatory animals. Accordingly, Xenacoelomorpha are more likely similar to Urbilateria rather than degenerated and simplified coelomate deuterostomes. If so, the ground pattern of Bilateria has been retained only partially in the remaining main bilaterian clades (Nephrozoa) after the deviation of the Xenacoelomorpha, namely the nervous system in the Deuterostomia and the body cavity conditions in the acoelomate Lophotrochozoa (particularly Platyzoa), Gastrotricha and cycloneuralian Ecdysozoa.     

The Biphasic Life Cycle--A Central Theme of Metazoan Evolution

SYNOPSIS. A life cycle alternating between a microscopic larva(mmsized) and macroscopic adult (cm-sized) occurs commonly amonginvertebrates. The pattern of occurrence of such a biphasiclife cycle among lower metazoans like the Porifera and Cnidaria,as well as ultrastructure of larva and adults of many invertebrates,suggests that the earliest phases of metazoan evolution alsohad such a cycle. Only the dispersive larvae in the originalmetazoans could be characterized as "small and mobile" if wefollow this model to its logical conclusion; the adults, bycontrast, evolved into larger-bodied organisms to maximize reproductionand were non-motile filter feeders for the most part. The biphasiclife cycle arose early in evolution, then, shortly after thefirst multicellular organisms evolved as clones of flagellatedcells linked together by interactions through ECM; selectivepressures acting independently on the two phases of the lifecycle led to the origin of the different metazoan tissue types—epithelial,connective, nervous, and muscle tissues. For the Bilateria,this suggests that extant acoelomate and pseudocoelomate formsevolved through progenesis of larvae and juveniles in a mannerlike that known for the radiation of the interstitial annelids.A better understanding of larval biology and of mechanisms forheterochrony is crucial for hypotheses of metazoan evolution.     

The Protonephridia of the Arctic Kinorhynch Echinoderes aquilonius (Cyclorhagida,Echinoderidae)

The cyclorhagid kinorhynch Echinoderes aquilonius Higgins & Kristensen, 1988 possesses a single pair of protonephridia located in segments 10 and 11. The protonephridia consist of: (1) three terminal cells T-1, T-2. T-3, each with two cilia; (2) a single non-ciliated canal cell; (3) a nephridiopore cell with many microvilli and a cuticular sieve plate. The protonephridia of Echinoderes are presumed to develop from the ectoderm near the area of the sieve plate on the eleventh segment, and are suspended in the dorso-lateral pseudocoelomic cavity where they are surrounded by a basal lamina. One of the terminal cells (T-1) secondarily penetrates the basal lamina of the tenth segment and a part of the cell attaches to the cuticle. The kinorhynch protonephridia are compared with the excretory organs of other Bilateria. expecially the ‘aschelminths’, and apomorphic characters of the kinorhynch protonephridia are defined.