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

Abstract

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

O anus, where art thou? An investigation of ctenostome bryozoans

“…Numerous issues remain open for future studies, including: morphology of the digestive tract and correlation with the position of the anus, general diversity of cheilostome guts, and study of live animals, especially ctenostomes with vestibular anuses. Along with other increasing data on soft tissue morphology (Schwaha, 2019a(Schwaha, , 2019bSchwaha et al, 2020), the position of the anus is an important character for phylogenetic inferences as it does not seem to correlate with zooidal or colonial characters. Molecular trees of ctenostomes just start to appear (e.g., Waeschenbach, Vieira, Reverter-Gil, Souto-Derungs, Nascimento, & Fehlauer-Ale, 2015) and once a new and more complete phylogenetic tree of ctenostome bryozoans is available, it should become clearer how often a vestibular anus has evolved.…”

“…This restricted range of protrusion is related to the morphological design of cyclostomes. They (and probably all stenolaemates) evolved a unique protrusion mechanism by detaching their peritoneal lining from the remaining body wall to form the socalled membranous sac (Borg, 1926;Ernst, 2019;Schwaha et al, 2020). Proximally, the membranous sac is connected to the F I G U R E 3 Schematic drawing of lophophore density and effects of a lophophoral and vestibular anus indicated by faeces in brown for the former and turquoise for the latter.…”

“…The digestive tract of bryozoans is U-shaped and divided into three distinct areas: foregut, midgut, and hindgut. The latter terminates via the anus in the tentacle sheath (Silén, 1944, Schwaha et al, 2020, see also Figure 1).…”

First evidence of virus-like particles in the bacterial symbionts of Bryozoa

“…The phylum Bryozoa is comprised of active filterers that feed mainly on microscopic algae, gathering them out of seawater (Winston 1977, 1978; Shunatova & Ostrovsky 2001, 2002; Schwaha et al 2020). Together with sponges and cnidarians this group of colonial invertebrates is among the dominating foulers in many bottom communities from the intertidal zone to a depth of 8 km (Ryland 1970, 2005; McKinney & Jackson 1989; Nielsen 2013).…”

Are local dominance and inter-clade dynamics causally linked when one fossil clade displaces another?

“…Surprisingly, cheilostome origination rates have no detectable relationship to cyclostome origination or extinction rates, given the weights of the null model (columns 1, 3, model A). These results suggest consideration of additional factors such as potential key innovations (23,24) or environmental and ecological changes (14,25), that could reveal relationships to pulses of cheilostome radiation. Between rates of cheilostome and cyclostome extinction, a feedback model has the highest model weight (column 2, model D).…”