Modularity is the mother of invention: a review of polymorphism in bryozoans

Schack, Carolann; Gordon, Dennis P.; Ryan, Ken G.

doi:10.1111/brv.12478

Cited by 47 publications

(51 citation statements)

References 130 publications

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“…Polymorphic kenozooids present on the frontal wall increased protection of the colony, followed by the acquisition of protective frontal shields of various morphologies (Gordon, ; Gordon & Voigt, ; Lidgard et al ., ). Finally, highly complex morpho‐functional polymorphism led to the appearance of so‐called cormidial structures – zooidal complexes consisting of autozooids with adventitious avicularia and kenozooids forming their frontal shields, as well as the protective brood chamber (Lidgard et al ., ; Schack et al ., ). Such polymorphism evolved independently in all three main lineages of Myolaemata but is absent in Phylactolaemata.…”

Section: Key Novelties In Bryozoan Evolutionmentioning

confidence: 97%

“…There is morphofunctional specialization of zooids in a colony affecting either the cystids or polypides, or both. Feeding zooids are termed autozooids whereas zooids with other functions are termed autozooidal (with a functional polypide) or heterozooidal (polypide reduced) polymorphs (Silén, ; Cheetham & Cook, ; Lidgard et al ., ; Schack, Gordon & Ryan, ).…”

Section: Character Evolutionmentioning

confidence: 99%

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Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

2020

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Molecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter-feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well-developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre-dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore-cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum-oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U-shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.Biological Reviews 95 (2020) 696-729

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Section: Key Novelties In Bryozoan Evolutionmentioning

confidence: 97%

Section: Character Evolutionmentioning

confidence: 99%

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

2020

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“…Instead, they must obtain nutrients from neighboring autozooids via the funicular system (Mukai et al 1997). Although morphologically diverse, most avicularia are characterized by having an enlarged, hinged operculum-derived "mandible" that can be opened and shut with pairs of hypertrophied muscles (Winston 1984;Carter et al 2011;Schack et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Differential Gene Expression Between Polymorphic Zooids of the Marine BryozoanBugulina stolonifera

Treibergs¹,

Giribet²

2020

G3 Genes|Genomes|Genetics

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Bryozoans are a diverse phylum of marine and freshwater colonial invertebrates containing approximately 6,300 described living species. Bryozoans grow by budding new physiologically connected colony members (zooids) from a founding individual that forms from a metamorphosed larva. In some species these zooids come in different shapes and sizes and are specialized to serve different tasks within the. A complex interaction of genotype, environment, and developmental pathway shapes zooid fate, however, the specific mechanisms underlying the establishment of this division of labor remain unknown. Here, the first characterization of differential gene expression between polymorphic zooids of a bryozoan colony is presented. The development of different zooid types of lab-cultured Bugulina stolonifera colonies including feeding autozooids, avicularia (derived non-feeding zooids that are homologous to feeding autozooids but shaped like a bird's beak), and rhizoids (a branching network of non-feeding anchoring zooids) was explored using RNA sequencing, de novo transcriptome assembly, and differential gene expression analyses. High throughput sequencing of cDNA libraries yielded an average of 14.9 ± 1.3 (SE) million high-quality paired-end reads per sample. Data for the first de novo transcriptome assemblies of B. stolonifera and the first characterization of genes involved in the formation and maintenance of zooid types within a bryozoan colony are presented. In a comparison between autozooid and avicularium tissues, 1,097 significant differentially expressed genes were uncovered. This work provides a much-needed foundation for understanding the mechanisms involved in the development of polymorphic zooids and the establishment of division of labor in bryozoans.

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“…Zooid‐to‐zooid connections through the skeleton occur principally via pore plates, which permit the tissue strands of the metabolite‐transporting funiculus to pass from polypide to polypide (Banta, 1969). Cheilostomes typically have a higher diversity of polymorphs than extant cyclostomes (see review in Schack et al ., 2018b). As in cyclostomes, some cheilostomes undergo considerable secondary calcification, thickening the skeleton of the load‐bearing bases of erect colonies (McKinney & Jackson, 1989).…”

Section: Introductionmentioning

confidence: 99%

Skeletal resorption in bryozoans: occurrence, function and recognition

et al. 2020

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Skeletal resorption – the physiological removal of mineralised parts by an organism – is an important morphogenetic process in bryozoans. Reports of its occurrence and function across the phylum are patchy, however, and have not previously been synthesised. Here we show that resorption occurs routinely across a wide range of bryozoan clades, colony sizes, growth forms, ontogenetic stages, body wall types, skeletal ultrastructures and mineralogies. Beginning in the early Paleozoic, different modes and functions of resorption have evolved convergently among disparate groups, highlighting its utility as a morphogenetic mode in this phylum. Its functions include branch renovation, formation of branch articulations, excavation of reproductive chambers, part‐shedding, and creation of access portals for budding beyond previously formed skeletal walls. Bryozoan skeletons can be altered by resorption at microscopic, zooidal and colony‐wide scales, typically with a fine degree of control and coordination. We classified resorption patterns in bryozoans according to the morphology and function of the resorption zone (window formation, abscission or excavation), timing within the life of the skeletal element resorbed (primary or secondary), and scale of operation (zooidal or multizooidal). Skeletal resorption is probably greatly underestimated in terms of its utility and role in bryozoan life history, and its prevalence across taxa, especially in fossil forms. It is reported proportionally more frequently in stenolaemates than in gymnolaemates. Some modes of resorption potentially alter or remove the spatial–temporal record of calcification preserved within a skeleton. Consequently, knowledge that resorption has occurred can be relevant for some common applications of skeletal analysis, such as palaeoenvironmental interpretation, or growth and ageing studies. To aid recognition we provide scanning electron microscopy, backscattered electron scanning electron microscopy and transmission electron microscopy examples of skeletal ultrastuctures modified by resorption.

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Modularity is the mother of invention: a review of polymorphism in bryozoans

Cited by 47 publications

References 130 publications

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

Differential Gene Expression Between Polymorphic Zooids of the Marine BryozoanBugulina stolonifera

Skeletal resorption in bryozoans: occurrence, function and recognition

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