DNA Library of Life. Boyko B. Amin-Babjee S. Parasites of the spotted turtledove Streptopelia chinensis in Peninsular Malaysia. Malaysian Applied Biology 93— A preliminary survey of parasites of Malaysian red jungle fowl Gallus gallus spadiceus.
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Diagonal , E Barcelona, Spain. Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes excluding Acoelomorpha are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms.
Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis.
Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms. While some more basally branching groups - such as polyclad flatworms - retain the ancestral quartet spiral cleavage pattern, most flatworms have significantly diverged from this pattern and exhibit unique strategies to specify the common adult body plan. Most free-living flatworms i. Platyhelminthes excluding the parasitic Neodermata are directly developing, whereas in polyclads, also indirect developers with an intermediate free-living larval stage and subsequent metamorphosis are found.
A comparative study of developmental diversity may help understanding major questions in evolutionary biology, such as the evolution of cleavage patterns, gastrulation and axial specification, the evolution of larval types, and the diversification and specialization of organ systems.
In this review, we present a thorough overview of the embryonic development of the different groups of free-living turbellarian platyhelminths, including the Catenulida, Macrostomorpha, Polycladida, Lecithoepitheliata, Proseriata, Bothrioplanida, Rhabdocoela, Fecampiida, Prolecithophora and Tricladida, and discuss their main features under a consensus phylogeny of the phylum.
Flatworms Platyhelminthes are acoelomate, usually hermaphroditic, egg-laying bilaterians with multiciliated epithelial cells and are lacking a circulatory system, an anus and respiratory organs other than the epidermis [ 1 ]. The taxon is comprised of free-living and parasitic species, including flukes and tapeworms [ 2 ].
Since long, the embryonic development of flatworms has attracted attention of embryologists and phylogeneticists alike for their assumed central position in the evolution of the Bilateria or even the Metazoa [ 3 ].
Several hypotheses have been formulated to reconstruct the transition from ciliates to acoels [ 4 , 5 ], from cnidarian planula larvae to acoels [ 6 ] or from ctenophores to polyclads [ 7 ], and phylogenetic relationships were explored and discussed by studying the ontogeny of flatworms [ 3 ].
Today, the affiliation of the Platyhelminthes to the Spiralia or Lophotrochozoa , especially apparent in polyclad flatworms, is widely accepted and the problematic position of acoels and nemertodermatids, traditionally regarded as members of the Platyhelminthes see [ 8 ] and literature therein , is now commonly seen outside this phylum, either as sister group to all other bilaterians [ 9 ], as sister group of the Gnathostomulida [ 10 ] or as members of the deuterostomes [ 11 ].
Traditionally, two broad classifications were used to subdivide the Platyhelminthes. Here, we use the term "free-living flatworms" in the turbellarian sense, i. In addition, the structure of the oocyte was used as a systematic criterion. Flatworms with entolecithal eggs - eggs that contain all yolk needed for development - are called "Archoophora", and this condition is considered primitive or plesiomorphic, while the ectolecithy of the Neoophora all other platyhelminth taxa, including the Neodermata requires the invention of specialized yolk cell-producing organs, the vitellaria.
Besides the oocyte, ectolecithal eggs also incorporate extra-embryonic yolk cells within the egg capsule [ 2 , 3 , 12 - 14 ]. Diversity of body plans and phylogeny of free-living platyhelminthes.
Left side, consensus tree of various published phylogenetic reconstructions. The Catenulida is the sister group of the Rhabditophora [ 15 - 18 ], the Macrostomorpha the sister group to all other Rhabditophora [ 2 , 15 , 19 ].
The Polycladida is the sister group to the Neoophora [ 2 ], and the Lecithoepitheliata is sister group to all other Neoophora [ 2 , 20 ]. Subsequently, the Proseriata is the sister group of all other Neoophora except the Lecithoepitheliata [ 16 , 20 , 21 ], while the Neodermata is sister group to Rhabdocoela and Adiaphanida Fecampiida, Prolecithophora, Tricladida [ 15 , 16 , 20 , 21 ].
The Rhabdocoela is sister group to Adiaphanida [ 15 - 17 , 20 , 21 ]. Within the Adiaphanida, Fecampiida is sister group to Prolecithophora plus Tricladida [ 15 - 17 , 20 , 21 ]. According to Willems and coworkers, the Bothrioplanida is sister group to Adiaphanida plus Neodermata, although their overall tree topology is different than depicted here, where Bothrioplanida is sister group to the Eulecithophora [ 22 ].
Right side, live images of adult representatives of the major taxa of free-living flatworms with their developing embryos. Stenostomum sthenum with two developing zooids, fresh water, about 1 mm long. Macrostomum lignano , marine, about 1 mm long. Prosthiostomum siphunculus , marine, about 1 cm long. Several embryos per cocoon, several cocoons per egg plate.
Geocentrophora sphyrocephala , fresh water, about 1 mm long. No embryonic stage provided. Monocelis fusca , marine, about 1. Rhynchomesostoma rostratum , fresh water, about 1. Procerodes littoralis , marine, about 4 mm long. Cocoon about 1 mm in diameter. Lower left corner hatched juvenile. Anterior of adult specimens to the left. Cladistic phylogenies of the phylum were established by Karling [ 23 ], Ax [ 14 ], Ehlers [ 2 ] and Smith et al.
The three latter phylogenies already display the "Turbellaria" and the "Archoophora" to be paraphyletic by not encompassing all descendants of the same common ancestor, the Neodermata and the Neoophora, respectively, the monophyly of which is supported. In addition, they established some internal affinities that have been accepted until recently, such as the group Seriata, comprising of the Tricladida and Proseriata, or the Rhabdocoela, which previously included also the Neodermata.
In all these phylogenies, the Catenulida are regarded as the sister group to either only the Rhabditophora, or the Rhabditophora plus Acoelomorpha. The use of molecular data and more elaborate cladistic techniques confirmed the overall picture proposed by earlier studies, namely the paraphyly of "Turbellaria" and "Archoophora" and the monophyly of Neoophora and Neodermata, but showed that the relationships among particular groups of flatworms are in fact more complex.
Although some questions remain unanswered, e. The Acoelomorpha are no longer part of the Platyhelminthes proper, and Catenulida, Macrostomorpha and Polycladida are, possibly in this order, the most basally branching groups of flatworms, all of them showing entolecithal eggs. The Neoophora is comprised by the Lecithoepitheliata, the Proseriata, the Bothrioplanida, the Rhabdocoela, the Fecampiida, the Prolecithophora, the Tricladida and the Neodermata.
Similarly, the Rhabdocoela has experienced severe rearrangements [ 22 ], and Neodermata has become a separate group. The position of the Bothrioplanida previously considered to be proseriates [ 26 ] , however, is still not unambiguously resolved, as is the exact nature of the relationship between the Neodermata, the Adiaphanida, the Rhabdocoela and the Proseriata, or the relationship between the taxa within the Adiaphanida [ 16 , 22 , 25 ]. In a seminal work, the embryonic development of free-living flatworms known at the time was summarized and discussed by Bresslau [ 27 ], in particular comparing the "duet spiral cleavage" of acoels and the quartet spiral cleavage of polyclads with the more convoluted and unique development of rhabdocoels, triclads, Bothrioplana and Fecampia.
While polyclads follow a relatively stereotypical spiral cleavage pattern, in triclads and other neoophorans spiral cleavage was found to be replaced by a seemingly irregular disperse cleavage, referred to as " Blastomerenanarchie ". Quartet spiral cleavage was determined to be the most likely plesiomorphic cleavage pattern in platyhelminths, and four different types of development were proposed for the Neoophora, depending on their specific mode of encompassing the extra-embryonic yolk cells [ 3 ].
Later, the view that all Neoophora undergo an irregular cleavage pattern was changed by Giesa and Reisinger and coworkers [ 28 , 29 ]. They showed that neoophoran lecithoepitheliates and proseriates exhibit quartet spiral cleavage patterns despite the presence of extra-embryonic yolk cells within the egg, suggesting a gradual move away from spiral cleavage within the Neoophora [ 26 , 29 ].
They argue that several neoophoran taxa have originated independently from different archoophoran ancestors, explaining their different modes of engulfing the extra-embryonic yolk cells. The origin and formation of these so-called "hull cells" and its possible homology with the epibolic gastrulation of polyclads were considered central in reconstructing the evolution of developmental patterns in flatworms, as well as the nature of egg shell granules [ 30 ]. Nowadays, molecular techniques have complemented more classical embryological approaches, putting some representative species on the level of other emerging invertebrate model systems.
Herein, we review the existing literature dealing with the embryology of free-living Platyhelminthes sensu stricto , comprising the Catenulida and the Rhabditophora [ 17 ], under a consensus phylogeny. By doing so, we aim to create the adequate comparative framework in which testable hypotheses regarding the evolution and diversification of developmental modes in this phylum can be established.
In this part of the review, we provide the main findings on embryonic development in each of the main taxa of free-living flatworms, with particular focus on early development i. In the rest of the groups, organs develop from an embryonic blastema Emb. An-Veg means animal-vegetal axis and quad. The "Archoophora" Catenulida, Macrostomorpha and Polycladida is a paraphyletic group encompassing all flatworms with entolecithal eggs.
In entolecithal eggs, all yolk is contained within the oocytes. Archoophorans exhibit quartet spiral cleavage, at least during the early zygotic divisions. Knowledge of embryonic development in catenulids is scarce.
In the Macrostomorpha, development diverges from the 8-cell stage, with the formation of an external yolk mantle from the four vegetal yolky macromeres that eventually cover the embryo and will be later resorbed. The juvenile thereby develops from the inner mass of cells, which is organized into an embryonic blastema.
The Polycladida retain the normal quartet spiral cleavage, although some differences with other spiralian phyla e. Their development is determinative and gastrulation occurs through epiboly of the animal micromeres over the vegetal cells.
Some species of this group feature an intermediate larval phase. Catenulids are predominantly freshwater animals in the millimeter range with only about described species worldwide, about half of which are belonging to the genus Stenostomum [ 32 ].
Data about the embryonic development of catenulid species are few and far between. Observations on the embryonic development of the group have been undertaken with species of the genus Stenostomum , namely S.
Single oocytes are covered by either a thick [ 33 ] or thin [ 35 ] egg shell. Both in C. The first cleavage divisions can occur when the egg is still residing in the parent. At the 4-cell stage, the blastomere D divides first, so that a temporary 5-cell stage can be observed, before the 8- and then the cell stage are reached, which are described to look similar to polyclads of the same cell stage [ 35 ].
At the 2-cell stage, there is no marked size difference between the blastomeres, except when parts of a blastomere are being extruded into the periembryonic liquid [ 34 ]. Later embryonic stages following the diapause are not described yet for any catenulid. Interestingly, for Rhynchoscolex simplex , a so-called Luther's larva was described. While the embryonic development and the hatching could not be observed, in spring these larvae were found at the same location as later the adults.
The Macrostomorpha comprise small flatworms in the two taxa Haplopharyngida consisting of 2 marine species and Macrostomida about marine and freshwater species [ 32 ]. To present, studies on the embryonic development are restricted to the Macrostomida, and, with one exception Microstomum lineare , [ 35 ] , to the genus Macrostomum. Both single e. Macrostomum lignano and multiple up to 20, e.
Macrostomum romanicum embryos per egg shell or cocoon are deposited. Three polar bodies are extruded at the animal pole, which later become incorporated into the embryo Macrostomum appendiculatum, M. Large cytoplasmatic protuberances "blebbing" occur predominantly in the undivided oocyte, but are also seen during cleavage [ 35 , 37 , 38 ]. At the two-cell stage, one blastomere CD is usually slightly larger than the other AB , and by laeotropic left-handed division arrives at the four-cell-stage, where blastomere D is often, but not always largest.
The fourth cleavage is laeotropic again. The early cleavage pattern is of quartet spiral nature in macrostomids, as was shown in early accounts on M. Interestingly, in M. In Microstomum , cleavage was only observed up to the 8-cell stage [ 35 , 44 ]. Summary of the embryonic development of Macrostomorpha and Polycladida.
A-I , schematic representations of the early macrostomid modified from [ 43 ] and polyclad development adapted from [ 45 , 46 ].
Developmental diversity in free-living flatworms
It has had a significant negative impact on the rare endemic land snail faunas of some Pacific islands, and has become established in a wide variety of habitats. Movement between centres is probably restricted by quarantine measures targeting other pest species, for example restrictions on the movement of banana plants in northern Australia. Spread to native forest is probably largely restricted by the limited availability of a suitable moist habitat in adjacent agricultural areas, and the absence of preferred molluscan prey species. Molluscs are very uncommon in human-modified habitats in northern Australia. The accidental spread of the species can readily occur. One such transfer of the species in Australia is reported; the flatworm harboured in the hollow tuber of a houseplant Alocasia sent from Cardwell, Queensland, to Weipa, Cape York Peninsula Waterhouse and Norris, The invasiveness of the species in some Pacific countries is probably further promoted by the deliberate introduction as a biocontrol agent by humans, and the ready availability of preferred prey, such as Achatina and native mollusc species.
Diagonal , E Barcelona, Spain. Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes excluding Acoelomorpha are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms. Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis. Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms.
Land planarians Platyhelminthes, Geoplanidae are predatory soil-associated animals. Although small species generally less than 1 cm in length such as Microplana spp. Reports of invasive alien flatworms in Europe in recent years Sluys, include Arthurdendyus triangulatus from New Zealand, Platydemus manokwari originally from Papua New Guinea, Obama nungara from Brazil, and Parakontikia ventrolineata , Caenoplana coerulea , and Caenoplana bicolor from Australia see Table 1 for authors of taxa and key references. All these species are conspicuous animals, several centimetres in length. Five species were found, among which three can be attributed to known binomial taxa Bipalium kewense , B. This table provides complete information about authors and taxa and combination, thus making the general text lighter.