bioRxiv Science⌕ Search

Biology subjects

Gasiorowski, L.

Publications and source records attributed to Gasiorowski, L..

14 recordsLinked to original sources

Exotic catenulid flatworms (Platyhelminthes, Catenulida) and where to find them in a temperate climate - a field study in a botanic garden

Catenulids are free-living flatworms, common in eutrophic freshwaters such as ponds, ditches, or peatbogs, with most of the diversity described from tropical regions to date. Although the majority of the species have been described from warmer climates, most molecular studies have been done on specimens from temperate zones in Europe. We addressed this gap by sampling for exotic species in localities available in a temperate climate. In this study, we investigated catenulid diversity in the greenhouses at the University of Warsaw Botanic Garden and recorded two species known only from tropical areas (Stenostomum paraguayense and Suomina evelinae) and one exotic species recorded previously from a greenhouse in Poland (Stenostomum corderoi). Additionally, in the latter species, we provide evidence for environmentally induced coloration of sensory pits, which has not been reported thus far. We placed the collected species on a phylogeny using barcoding of 18S, 28S, and COI genes and retrieved paraphyly of the family Catenulidae, with S. evelinae forming a sister group to the genus Paracatenula, and hence we propose a revision of its systematic position. In total, we recorded six species, including three with a wide cosmopolitan distribution (C. turgida, S. grande and S. tuberculosum), and provided sequences for five of them, three of which had no previous molecular records (S. paraguayense, S. evelinae and S. corderoi). Thus, we confirm that greenhouses represent an important source of exotic species for taxonomic work on microscopic invertebrates.

zoology↗

Excessive feeding induces development of a colony-like body plan in paratomous flatworms

Colonial animals rely on agametic reproduction to generate repeated colony modules (zooids). Although zooid development has been extensively studied in fully colonial species, such as cnidarians, bryozoans, or tunicates, it provides limited insight into how and why animals transition from solitary asexual fission to colony formation. Here, we fill this gap by studying the dynamics of asexual development in the microscopic flatworm Stenostomum, which can alternate between asexual fission and colony-like linear chains, composed of several zooids connected tail-to-head. Combining ecological, developmental, physiological, and transcriptomic analyses, we demonstrate that in four species of Stenostomum, chain formation can be triggered by manipulating food availability. This ecological input changes the balance between somatic longitudinal growth and head morphogenesis rate, generating a transient modular organism without requiring a new developmental program. We found no evidence for division of labor among zooids or for enhanced predation avoidance of the worms in chains, indicating that chain formation might be a developmental byproduct without obvious adaptive value. Together, these findings suggest that a neutrally evolving developmental byproduct of food-modulated allometric growth may provide a mechanistic route from asexual reproduction to coloniality.

evolutionary biology↗

Divergent evolution of the Wnt signaling system in flatworms

Regenerative capacity varies widely across flatworms (Platyhelminthes). Whereas catenulids, microstomids and planarians can regenerate a complete head de novo, other flatworms cannot. This striking diversity raises a longstanding evolutionary question: does whole-body regeneration represent an ancestral trait that was subsequently lost in multiple lineages, or did it evolve convergently? Addressing this question requires comparative analyses of the molecular mechanisms underlying regeneration across phylogenetically diverse flatworms. Here, we focus on Wnt signaling, a deeply conserved regulator of antero-posterior (A-P) patterning and a central determinant of head-versus-tail identity during planarian regeneration, to establish a mechanistic framework for such comparisons. Although Wnt signaling has been studied extensively in planarians and parasitic neodermatans, its evolution and deployment in other flatworm clades remain poorly characterized. To address this gap, we characterized the complement of Wnt signaling components in two early-diverging flatworm clades, Catenulida and Macrostomorpha, with particular emphasis on expression and function in the catenulid Stenostomum brevipharyngium. Phylogenetic analyses reveal the ancient loss of six Wnt families and one secreted Frizzled-related protein (sFRP) family in the last common ancestor of flatworms, followed by additional lineage-specific gene losses and expansions. Moreover, several Wnt pathway components display markedly divergent expression patterns between catenulids and other flatworms, while functional analyses indicate corresponding differences in their regenerative deployment. Together, our findings reveal a dynamic evolutionary history of the flatworm Wnt signaling toolkit and establish a comparative framework for testing whether the molecular circuitry underlying head regeneration is ancestrally conserved or has evolved independently in distinct flatworm lineages.

evolutionary biology↗

Molecular phylogeny of Catenulida (Platyhelminthes) with special focus on their diversity in Poland

Catenulida is a clade of free-living flatworms found abundantly in freshwater habitats across the globe. Despite their ubiquitous distribution, catenulids remain poorly studied; most of the species are known only from the asexual forms that lack distinct, taxonomically useful characters. Accordingly, the studies of catenulid diversity require application of integrative methods that combine morphological and molecular data. Here, we report the survey of catenulid diversity in Central and Western Europe, with a special focus on the species found in Polish freshwaters. We collected and identified 13 distinct morphotypes that were subsequently sequenced for four molecular markers - 18S, 28S, COI and ITS-5.8S. The obtained sequences, together with reference data from other catenulid species, were used to infer the comprehensive phylogeny of the clade. The analysis revealed several well-supported clades within the largest catenulid family, Stenostomidae, highlighting the major challenges in catenulid taxonomy, such as unresolved species complexes of Stenostomum leucops and Stenostomum simplex. By tracing evolution of morphological, developmental and ecological characters on the phylogeny our study provides insight into major character transitions in the key lineages of catenulids.

zoology↗

Spontaneous ectopic head formation enables reversal of the body axis polarity in microscopic flatworms

In most of the animals the antero-posterior axis is specified during early embryogenesis. However, in the organisms that undergo somatic asexual reproduction constant re-establishment of the body axis occurs during each asexual act in the context of the fully formed adult body. In microscopic flatworms from the genus Stenostomum the new head and tail structures are inserted in the pre-existing body plan during the asexual process known as paratomy. Here, we report a spontaneously occurring developmental error that results in the formation of the worms with double heads at the opposite ends of their bodies that misses the posterior pole identity. In the set of experiments, we show that the double head phenotype is not heritable on the organismal level. Worms originating from the sectioning or fission of the double head animals give rise to the healthy populations that do not display the erroneous asexual development. We also demonstrate that the posterior piece of the double head worm can survive, regenerate the tail on its previously anterior pole and resume the asexual reproduction. Effectively, such regeneration allows reversal of the body axis polarity without impairment of the survival or reproductive abilities of the animal, an exceptionally rare phenomenon among bilaterians.

developmental biology↗

An integrative taxonomic approach reveals unexplored diversity in Croatian planarians

BackgroundFreshwater ecosystems are among the most endangered habitats on Earth, with approximately one-fourth of aquatic species at risk of extinction. Effective conservation efforts require comprehensive monitoring and accurate species identification, including often overlooked groups. DNA barcoding promises rapid and accessible species identification but requires the availability of "universal" primer pairs and robust, taxonomically curated reference libraries. Planarian flatworms are one such group for which these resources are currently lacking, even though they are common constituents of freshwater ecosystems worldwide. As a result, the true extent of planarian diversity remains underappreciated in many areas. ResultsMotivated by the highly skewed representation of planarian diversity in current GenBank records of the barcoding gene mitochondrial cytochrome c oxidase subunit I (COI), we optimised existing barcoding primers and tested them on planarians collected in a species-rich but, so far, poorly surveyed region of Croatia. Using an integrative approach combining the new primers, traditional taxonomy and karyology, we generated new taxonomically curated COI barcode sequences for European dugesiids, dendrocoelids and planariids, which, in the case of the latter two groups, represent a substantial increase of the number of entries for those families. Our efforts resulted in several significant findings, including the description of a new pigmented Dendrocoelum species, Dendrocoelum pigmentatum sp. nov, the discovery of two highly differentiated haplotypic clades in Schmidtea lugubris, and the rediscovery of Polycladodes alba in Croatia after a century. ConclusionsOverall, our work extends the utility of DNA barcoding for species-level identification of planarians to previously inaccessible groups. Additionally, it integrates Croatia as an underexplored but species-rich region into the endeavour to systematically describe the planarian fauna of Europe. The expansion of a known number of Croatian planarian species from eight to sixteen and the discovery of a new, large planarian species in continental Europe, Dendrocoelum pigmentatum, demonstrate the effectiveness of our integrative approach. Overall, our work highlights the underappreciated diversity of planarians, even in continental Europe and supports practical conservation efforts to preserve aquatic biodiversity.

zoology↗

Evidence for multiple independent expansions of Fox gene families within flatworms

Expansion and losses of gene families are important drivers of molecular evolution. A recent survey of Fox genes in flatworms revealed that this superfamily of multifunctional transcription factors, present in all animals, underwent extensive losses and expansions during platyhelminth evolution. In this paper, I analyzed Fox gene complement in four additional species of platyhelminths, that represent early-branching lineages in the flatworm phylogeny: catenulids (Stenostomum brevipharyngium and Stenostomum leucops) and macrostomorphs (Macrostomum hystrix and Macrostomum cliftonense). Phylogenetic analysis of Fox genes from this expanded set of species provided evidence for multiple independent expansions of Fox gene families within flatworms. Notably, FoxG, a panbilaterian brain-patterning gene, appears to be the least susceptible to duplication, while FoxJ1, a conserved ciliogenesis factor, has undergone extensive expansion in various flatworm lineages. Analysis of the single-cell atlas of S. brevipharyngium, combined with RNA in situ hybridization, elucidated the tissue-specific expression of the selected Fox genes: FoxG is expressed in the brain, three of the Fox genes (FoxN2/3-2, FoxO4 and FoxP1) are expressed in the pharyngeal cells of likely glandular function, while one of the FoxQD paralogs is specifically expressed in the protonephridium. Overall, the evolution of Fox genes in flatworms appears to be characterized by an early contraction of the gene complement, followed by lineage-specific expansions that have enabled the co-option of newly evolved paralogs into novel physiological and developmental functions. Statements and DeclarationsThe author has no competing interests to declare that are relevant to the content of this article. The research was funded by the Alexander von Humboldt Foundation (The Humboldt Research Fellowship for Postdoctoral Researchers) and The Polish National Agency for Academic Exchange (Polish Returns NAWA grant no. BPN/PPO/2023/1/00002).

evolutionary biology↗

Regeneration in the absence of canonical neoblasts in an early branching flatworm

The remarkable regenerative abilities of flatworms are closely linked to neoblasts - adult pluripotent stem cells that are the only division-competent cell type outside of the reproductive system. Although the presence of neoblast-like cells and whole-body regeneration in other animals has led to the idea that these features may represent the ancestral metazoan state, the evolutionary origin of both remains unclear. Here we show that the catenulid Stenostomum brevipharyngium, a member of the earliest-branching flatworm lineage, lacks conventional neoblasts despite being capable of whole-body regeneration and asexual reproduction. Using a combination of single-nuclei transcriptomics, in situ gene expression analysis, and functional experiments, we find that cell divisions are not restricted to a single cell type and are associated with multiple fully differentiated somatic tissues. Furthermore, the cohort of germline multipotency genes, which are considered canonical neoblast markers, are not expressed in dividing cells, but in the germline instead, and we experimentally show that they are neither necessary for proliferation nor regeneration. Overall, our results challenge the notion that canonical neoblasts are necessary for flatworm regeneration and open up the possibility that neoblast-like cells may have evolved convergently in different animals, independent of their regenerative capacity.

zoology↗

Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid-bryozoan stem lineage

BackgroundBrachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicates that both groups are descended from biomineralising Cambrian ancestors, the closest relatives of brachiopods - phoronids and bryozoans - are mineralised to a much lower extent and are comparatively poorly represented in the Palaeozoic fossil record. Although brachiopod and mollusc shells are structurally analogous, genomic and proteomic evidence indicates that their formation involves a complement of conserved, orthologous genes. Here, we study a set of genes comprised of three homeodomain transcription factors, one signalling molecule and 6 structural proteins which are implicated in mollusc and brachiopod shell formation, search for their orthologs in transcriptomes or genomes of brachiopods, phoronids and bryozoans, and present expression patterns of 8 of the genes in postmetamorphic juveniles of the rhynchonelliform brachiopod Terebratalia transversa. ResultsTranscriptome and genome searches for the 10 target genes in the brachiopods T. transversa, Lingula anatina, Novocrania anomala, the bryozoans Bugula neritina and Membranipora membranacea, and the phoronids Phoronis australis and Phoronopsis harmeri resulted in the recovery of orthologs of the majority of the genes in all taxa. While the full complement of genes was present in all brachiopods with a single exception in L. anatina, a bloc of four genes could consistently not be retrieved from bryozoans and phoronids. The genes engrailed, distal-less, ferritin, perlucin, sp1 and sp2 were shown to be expressed in the biomineralising mantle margin of T. transversa juveniles. ConclusionsThe gene expression patterns we recovered indicate that while mineralised shells in brachiopods and molluscs are structurally analogous, their formation builds on a homologous process that involves a conserved complement of orthologous genes. Losses of some of the genes related to biomineralisation in bryozoans and phoronids indicate that loss of the capacity to form mineralised structures occurred already in the phoronid-bryozoan stem group and supports the idea that mineralised skeletons evolved secondarily in some of the bryozoan subclades.

developmental biology↗

Gene expression in the developing nemertean brain indicates convergent evolution of complex brains in Spiralia

BackgroundNemertea is a clade of worm-like animals, which belongs to a larger animal group called Spiralia (together with e.g. annelids, flatworms and mollusks). Many of the nemertean species possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been suggested as homologues to the annelid mushroom bodies. In order to understand the developmental and evolutionary origins of complex nemertean brain, we investigated details of neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber. ResultsIn the hatched juveniles the CNS is already composed of all major elements present in the adults, including the brain (with dorsal and ventral lobes), paired longitudinal lateral nerve cords and an unpaired dorsal nerve cord. The TEM investigation of the juvenile cerebral organ revealed that the structure is already composed of several distinct cell types present also in the adults. We further investigated the expression of twelve transcription factors commonly used as brain and cell type markers in bilaterian brains, including genes specific for annelid mushroom bodies. The expression of the investigated genes in the brain is region-specific and divides the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, we detected expression of mushroom body specific genes in the developing cerebral organs. ConclusionsAt the moment of hatching, the juveniles of L. ruber already have a similar neuroarchitecture as adult worms, which suggests that further neural development is mostly related with increase in the size but not in complexity. Comparison in the gene expression between L. ruber and the annelid Platynereis dumerilii and other spiralians, indicates that the complex brains present in those two species evolved convergently by independent expansion of non-homologues regions of the simpler brain present in their common ancestor. The similarities in gene expression in mushroom bodies and cerebral organs might be a result of the convergent recruitment of the same genes into patterning of non-homologues organs or the results of more complicated evolutionary processes, in which conserved and novel cell types contribute to the non-homologues structures.

evolutionary biology↗

A single origin of animal excretory organs

Excretion is an essential physiological process, carried out by all living organisms regardless of their size or complexity(1-3). Most animals, which include both protostomes (e.g. flies, flatworms) and deuterostomes (e.g. humans, sea urchins) (together Nephrozoa(4, 5)), possess specialized excretory organs. Those organs exhibit an astonishing diversity, ranging from units composed of just three distinct cells (e.g. protonephridia) to complex structures, built by millions of cells of multiple types with divergent morphology and function (e.g. vertebrate kidneys)(6, 7). Although some molecular similarities between the development of kidneys of vertebrates and the regeneration of the protonephridia of flatworms have been reported(8, 9), the molecular development of nephrozoan excretory organs has never been systematically studied in a comparative context(6). Here we show that a set of highly conserved transcription factors and structural proteins is expressed during the development of excretory organs of six species that represent major protostome lineages and non-vertebrate deuterostomes. We demonstrate that the molecular similarity witnessed in the vertebrate kidney and flatworm protonephridia(8) is also seen in the developing excretory organs of other Nephrozoa. In addition, orthologous structural proteins forming the ultrafiltration apparatus are expressed in all these organs in the filter-forming cells. Our results strongly suggest that excretory organs are homologous and are patterned by the conserved set of developmental genes. We propose that the last common nephrozoan ancestor possessed an ultrafiltration-based, ciliated excretory organ, a structure that later gave rise to the vast diversity of extant excretory organs, including the human kidney. Significance statementMost of the bilaterally symmetrical animals excrete through specialized excretory organs, such as kidneys and nephridia. However, due to the morphological diversity of these organs, it remains unknown whether those structures evolved from a common ancestral organ or appeared several times independently during evolution. In order to answer the question about the origin of excretory organs we investigated the molecular pathways and structural genes involved in the development of nephridia in 6 animal species representing major evolutionary lineages. We show that diverse excretory organs share an ancient molecular patterning and structural molecules. Our results provide strong evidence that all excretory organs originated from a single, simple organ that performed urine production by ultrafiltration in deep geological past.

evolutionary biology↗

Hox gene expression during the development of the phoronid Phoronopsis harmeri

BackgroundPhoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri.\n\nResultsWe identified sequences of 8 Hox genes in the transcriptome of P. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. The Hox genes are expressed in the metasomal sac, posterior mesoderm and junction between midgut and hindgut - structures that represent rudiments of the adult worm, which emerges through the process of drastic metamorphosis. Additionally, two Hox genes are expressed in the posterior telotroch, which develops in the later larval stages.\n\nConclusionsThe lack of Hox gene expression during early development of P. harmeri indicates that the larval body develops without positional information of the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral, direct life cycle of phoronids. Accordingly, the specific actinotrocha larva found only in Phoronida, would represent an evolutionary novelty, for which an alternative molecular mechanism of antrerior-posterior patterning was recruited. Another explanation of the observed Hox gene expression is that the actinotrocha represents a \"head larva\", which is composed of the most anterior body region that is devoid of Hox gene expression. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. Future investigation on head-specific genes expression is needed to test this hypothesis.

developmental biology↗

Morphology of the nervous system of monogonont rotifer Epiphanes senta with focus on sexual dimorphism between feeding females and dwarfed males

BackgroundMonogononta is a large clade of rotifers comprised of diverse morphological forms found in a wide range of ecological habitats. Most of the monogonont species display a cyclical parthenogenesis, where generations of asexually reproducing females are interspaced by mixis events when sexual reproduction occurs between mictic females and dwarfed, haploid males. The morphology of monogonont feeding females is relatively well described, however data on male anatomy are very limited. Thus far, male musculature of only two species has been described with confocal laser scanning microscopy (CLSM) and it remained unknown how dwarfism influences neuroanatomy of males.\n\nResultsHere, we provide a CLSM-based description of the nervous system of both sexes of Epiphanes senta, a freshwater monogonont rotifer. The general nervous system architecture is similar between males and females and shows same level of complexity. However, the nervous system in males is more compact and lacks its stomatogastric part.\n\nConclusionComparison of the neuroanatomy between male and normal-sized feeding females provides better understanding of the nature of male dwarfism in Monogononta. We propose that dwarfism of monogonont non-feeding males is a specific case of progenesis as they, due to their inability to feed, retain a juvenile body size. Reduction of the stomatogastric nervous system in the males correlates with the loss of entire digestive tract and associated morphological structures.

zoology↗

Hox gene expression in postmetamorphic juveniles of the brachiopod Terebratalia transversa

BackgroundHox genes encode a family of homeodomain containing transcription factors that are clustered together on chromosomes of many Bilateria. Some bilaterian lineages express these genes during embryogenesis in spatial and/or temporal order according to their arrangement in the cluster, a phenomenon referred to as collinearity. Expression of Hox genes is well studied during embryonic and larval development of numerous species; however, relatively few studies focus on the comparison of pre- and postmetamorphic expression of Hox genes in animals with biphasic life cycle. Recently, the expression of Hox genes was described for embryos and larvae of Terebratalia transversa, a rhynchonelliformean brachiopod, which possesses distinct metamorphosis from planktonic larvae to sessile juvenile. During premetamorphic development, T. transversa does not exhibit spatial collinearity and several of its Hox genes are recruited for the morphogenesis of novel structures. In our study we determined expression of Hox genes in post-metamorphic juveniles of T. transversa in order to examine metamorphosis-related changes of expression patterns and to test if Hox genes are expressed in the spatially collinear way in the postmetamorphic juveniles.\n\nResultsHox genes are expressed in a spatially non-collinear manner in juveniles, generally showing similar patterns as ones observed in competent larvae: genes labial and Post1 are expressed in chaetae-related structures, sex comb reduced in the shell forming epithelium, whereas Lox5 and Lox4 in dorso-posterior epidermis. After metamorphosis expression of genes proboscipedia, Hox3, Deformed and Antennapedia becomes restricted to, respectively, shell musculature, prospective hinge rudiments, and pedicle musculature and epidermis.\n\nConclusionsAll developmental stages of T. transversa, including postmetamorphic juveniles, exhibit a spatial non-collinear Hox genes expression with only minor changes observed between pre- and postmetamorphic stages. Our results are concordant with morphological observation that metamorphosis in rhynchonelliformean brachiopods, despite being rapid, is rather gradual. The most drastic changes in Hox genes expression patterns observed during metamorphosis could be explained by the inversion of the mantle lobe, which relocates some of the more posterior larval structures into the anterior edge of the juveniles. Cooption of Hox genes for the morphogenesis of novel structures is even more pronounced in post-metamorphic brachiopods when compared to larvae.

developmental biology↗