Diversity of brood chambers in calloporid bryozoans (Gymnolaemata,Cheilostomata): comparative anatomy and evolutionary trends

Comparative anatomical studies of 12 species from 10 genera (Callopora, Tegella, Amphiblestrum, Parellisina, Corbulella, Crassimarginatella, Valdemunitella, Bryocalyx, Concertina, Cauloramphus) belonging to one of the largest and most diverse bryozoan taxa, the Calloporidae, and one species from the genus Akatopora belonging to the related taxon Antroporidae, were undertaken to elucidate the morphological diversity of brooding structures and to recognize main trends in their evolution. Most of the species studied possess ovicells (specialized brooding receptacles) formed by the distal and maternal (egg-producing) autozooids. The distal zooid can be an autozooid, a vicarious avicularium or a kenozooid. The calcified protective hood (ooecium) is an outgrowth from the distal zooid. Hyperstomial or prominent ovicells are most common. They were found in species of the genera Callopora, Tegella, Amphiblestrum, Parellisina, Corbulella, Bryocalyx and Concertina. Subimmersed ovicells were found in Valdemunitella, and immersed ovicells in Crassimarginatella and Akatopora. Cauloramphus has an internal brooding sac and a vestigial kenozooidal ooecium, budded by the maternal zooid. Based on the structure of the brooding organs, the following evolutionary trends can be recognized within the group: (1) reduction of the distal (ooecium-producing) zooid, (2) immersion of the brooding cavity correlated with a reduction of the ooecium and ooecial vesicle and with changes in the ovicell closure and the structure of the brood chamber floor, (3) reduction of the calcification of the ectooecium, and (4) transition from bilobate to entire ooecium. The trend towards immersion of the brooding cavity could have evolved repeatedly within the Calloporidae. Transition from bilobate to entire ooecium is characteristic of the related taxon Cribrilinidae, showing a good example of parallel evolution of the ooecium in two closely related clades. Possible causes for the transformations described are discussed.     

Comparative Studies of Ovicell Anatomy and Reproductive Patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida)

Investigations of the common boreal-arctic cheilostomate bryozoans Cribrilina annulata and Celleporella hyalina have shown that the two species possess similar ovicell structures and reproductive patterns. Both species are characterized by frontal dwarf ovicellate zooids, that are female autozooidal polymorphs in C. hyalina and simultaneous hermaphroditic autozooids in C. annulata. The latter species in addition has ovicellate autozooids of the usual type. Each ovicell is formed from a maternal zooid only, and its cavity is lined by the outer hemispherical fold (ooecium) and the distal zooidal wall. The coelomic cavity of the ooecium is separated from the body cavity of the maternal zooid by a transverse wall with simple pores. Each pore is closed by a cell plug, and the ooecia may be considered as kenozooids. Each oocyte is accompanied by a single nurse cell that degenerates after ovulation. The eggs are macrolecithal in C. annulata and microlecithal in C. hyalina, and the former species is a non-placental brooder whereas the latter forms a placenta. Fertilization is precocious. Possible mechanisms of sperm entry as well as oviposition are discussed. The literature concerning ovicell structure and development in cheilostomates is analysed. It is proposed that the brood chamber of cribrimorphs evolved by a fusion of costae and a reduction of the daughter zooid in ancestral forms. © 1998 The Royal Swedish Academy of Sciences. Published by Elsevier Science Ltd. All rights reserved     

Ovicell structure in Callopora dumerilii and C. lineata (Bryozoa: Cheilostomatida)

Anatomical and SEM-studies of the brood-chambers (ovicells) in two bryozoans (Callopora dumerilii and C. lineata) were undertaken to resolve a long-term controversy existing in the literature about the origin of the ovicells. In contrast with the interpretation of Silén (1945 ), both species investigated possess hyperstomial ovicells with the ooecium formed by the distal (daughter) zooid. The ooecial coelomic cavity communicates with the zooidal coelom through a pore-like canal or canals remaining after the closure of an arch-shaped slit. The slit forms during ovicellogenesis. The communication canals are normally plugged by epithelial cells, however incompletely closed canals were also found in Callopora lineata. SEM-studies of noncleaned, air-dried specimens showed a relationship between membranous and calcified parts during early ovicellogenesis. It starts from a transverse wall as the calcification of the proximal part of the daughter zooid frontal wall, and has the shape of two flat rounded plates. There are no knobs or any other outgrowths. Conditions and phenomenology of hyperstomial ovicell formation are discussed.     

Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomic and evolutionary implications

The anatomical structure of internal sacs for embryonic incubation was studied using SEM and light microscopy in three cheilostome bryozoans-Nematoflustra flagellata (Waters,1904), Gontarella sp., and Biflustra perfragilis MacGillivray, 1881. In all these species the brood sac is located in the distal half of the maternal (egg-producing) autozooid, being a conspicuous invagination of the body wall. It consists of the main chamber and a passage (neck) to the outside that opens independently of the introvert. There are several groups of muscles attached to the thin walls of the brood sac and possibly expanding it during oviposition and larval release. Polypide recycling begins after oviposition in Gontarella sp., and the new polypide bud is formed by the beginning of incubation. Similarly, polypides in brooding zooids degenerate in N. flagellata and, sometimes, in B. perfragilis. In the evolution of brood chambers in the Cheilostomata, such internal sacs for embryonic incubation are considered a final step, being the result of immersion of the brooding cavity into the maternal zooid and reduction of the protecting fold (ooecium). Possible reasons for this transformation are discussed, and the hypothesis of Santagata and Banta (Santagata and Banta1996) that internal brooding evolved prior to incubation in ovicells is rejected.     

Brood chambers constructed from spines in fossil and Recent cheilostome bryozoans

Most cheilostome bryozoans brood their larvae in skeletal structures called ovicells which, in evolutionary terms, were derived from spines. Ovicells in the great majority of fossil and Recent cheilostomes, however, have lost all or most traces of their spinose origin. Here we review the occurrence of spinose (including costate) brood chambers in cheilostomes, investigating in detail 32 species belonging to ten genera among five families (Calloporidae, Monoporellidae, Macroporidae, Cribrilinidae and Tendridae). Spinose ovicells are moderately common in the Upper Cretaceous, where they are recorded in 28 species, and also occur in one Palaeocene, seven Eocene‐Miocene and 11 Recent species. The most primitive cheilostome ovicells occur in mid‐Cretaceous calloporids in which a group of mural spines belonging to the distal zooid were apparently bent towards the maternal zooid to form a cage‐like structure for reception of the embryo. The bases of these spines were initially aligned in a distally concave row that later became straight, distally convex and finally horseshoe‐shaped, affording progressively better protection for the developing embryo. We suggest that primitive monoporellids inherited from calloporid ancestors a distally concave arrangement of ovicell spine bases, while cribrilinids inherited a horseshoe‐shaped arrangement. Important trends that can be recognized in early ovicell evolution include: (1) loss of basal spine articulation; (2) spine flattening; (3) closure of the gaps between spines; (4) reduction in spine number (through loss or fusion), and (5) development of a concave ovicell floor. The conventional ‘unipartite’ ovicells found in the majority of cheilostomes may have originated either by spine fusion, as seems likely in some cribrilinids, or through a progressive loss of spines via an intermediate stage, seen in some calloporids and in two monoporellids, where the ovicell comprises a large pair of flattened spines. The spinose ovicells of some monoporellids and macroporids subsequently evolved investments of hypostegal coelom that allowed secretion of a surface layer of cryptocystal calcification. Acanthostegous brood chambers characteristic of Tendridae apparently provide an example of independent evolution of spinose brooding structures. © 2005 The Natural History Museum, London, Zoological Journal of the Linnean Society, 2005, 144 , 317?361.     

Systematics of Upper Cretaceous calloporid bryozoans with primitive spinose ovicells

The majority of fossil and Recent cheilostome bryozoans brood their larvae in ovicells. These double-walled, hood-like skeletal structures are thought to have arisen through modification of spines belonging to the zooid distal of the maternal zooid. Support for this hypothesis comes from the existence of ovicells constructed of multiple spines in a few Upper Cretaceous species belonging to two groups, microporids and cribrimorphs. Here we report the discovery of similar multispinose ovicells in a third group, calloporids, which are closely related to primitive cheilostomes that do not brood their larvae. The genus Distelopora Lang, 1915 from the Cenomanian ('Chalk Marl') of Cambridge is taken out of synonymy and shown to comprise the type species ( D. bipilata ) and two new species ( D. langi and D. spinifera ) of multiserial calloporids. Between 5 and 15 spine bases are arranged in a crescent on the gymnocyst of the zooid distal of each maternal (egg-producing) zooid in Distelopora . This indicates the presence of an ovicell formed by a cage of basally articulated spines. Similar ovicells represented by 18–19 spine bases occur in a uniserial calloporid from the German Campanian Allantopora krauseae Voigt and Schneemilch, 1986, which is made the type species of the new genus Unidistelopora . Another calloporid from the Cambridge Cenomanian has ovicells constructed by two claw-like, flattened, non-articulated and laterally juxtaposed spines. Described as Gilbertopora larwoodi gen. et sp. nov., this multiserial species provides a link between Distelopora and more typical cheilostome ovicells. The spines forming primitive ovicells provide a good example of exaptations, co-opted from their original function protecting the polypide of the distal zooid.     

Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free‐living cheilostomes

Numerous gross morphological attributes are shared among unrelated free‐living bryozoans revealing convergent evolution associated with functional demands of living on soft sediments. Here, we show that the reproductive structures across free‐living groups evolved convergently. The most prominent convergent traits are the collective reduction of external brood chambers (ovicells) and the acquisition of internal brooding. Anatomical studies of four species from the cheilostome genera Cupuladria and Discoporella (Cupuladriidae) show that these species incubate their embryos in internal brooding sacs located in the coelom of the maternal nonpolymorphic autozooids. This sac consists of a main chamber and a narrow neck communicating to the vestibulum. The distal wall of the vestibulum possesses a cuticular thickening, which may further isolate the brood cavity. The presence of this character in all four species strongly supports grouping Cupuladria and Discoporella in one taxon. Further evidence suggests that the Cupuladriidae may be nested within the Calloporidae. Based on the structure of brooding organs, two scenarios are proposed to explain the evolution of the internal brooding in cupuladriids. The evolution of brood chambers and their origin in other free‐living cheilostomes is discussed. Unlike the vast majority of Neocheilostomina, almost all free‐living cheilostomes possess nonprominent chambers for embryonic incubation, either endozooidal and immersed ovicells or internal brooding sacs, supporting the idea that internal embryonic incubation is derived. We speculate that prominent skeletal brood chambers are disadvantageous to a free‐living mode of life that demands easy movement through sediment in instable sea‐floor settings. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata)

Background

Matrotrophy or extraembryonic nutrition ?C transfer of nutrients from mother to embryo during gestation ?C is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.

Results

Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.

Conclusions

The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.     

Ultrastructure and Development of the Ooecial Walls in Some Calloporid Bryozoans (Gymnolaemata: Cheilostomata)

In the brood chambers (ovicells) of six calloporid cheilostomes studied each skeletal wall consists of four calcified layers: (1) a very thin superficial layer of planar spherulitic crystallites, (2) an upper (outer) layer with wall-perpendicular prismatic ultrastructure, (3) an intermediate lamellar layer, and (4) a lower (inner) wall-perpendicular prismatic layer. Comparative studies of both the ovicell wall ultrastructure and early ovicell formation showed a hypothetical opportunity for evolving complex (multilayered) skeletal walls by fusion of the initially separated gymnocystal and cryptocystal calcifications in Cheilostomata. In two species studied, a bilobate pattern in the final stage of the formation of the ooecial roof was encountered in specimens with the cuticle preserved. A possible explanation to this finding is discussed – the bilobate pattern is suggestive of the hypothetical origin of the brood chamber from (1) two flattened spines, or (2) reduction in spine number of an originally multispinous ovicell.     

Multizooidal Budding in Parasmittina trispinosa (Johnston) (Bryozoa,Cheilostomata)

Two principally different wall types occur in the bryozoan colony: Exterior walls delimiting the super-individual, the colony, against its surroundings and interior walls dividing the body cavity of the colony thus defined into units which develop into sub-individuals, the zooids. In the gymnolaemate bryozoans generally, whether uniserial or multiserial, the longitudinal zooid walls are exterior, the transverse (proximal and distal) zooid walls interior ones. The radiating zooid rows grow apically to form “tubes” each surrounded by exterior walls but subdivided by interior (transverse) walls. The stenolaemate bryozoans show a contrasting mode of growth in which the colony swells in the distal direction to form one confluent cavity surrounded by an exterior wall but internally subdivided into zooids by interior walls. In the otherwise typical gymnolaemate Parasmittina trispinosa the growing edge is composed of a series of “giant buds” each surrounded by exterior walls on its lateral, frontal, basal and distal sides and forming an undifferentiated chamber usually 2–3 times as broad and 3 or more times as long as the final zooid. Its lumen is subdivided by interior walls into zooids 2–3, occasionally 4, in breadth. This type of zooid formation is therefore similar to the “common bud” or, better-named, “multizooidal budding” characteristic of the stenoleamates but has certainly evolved independently as a special modification of the usual gymnolaemate budding.     

Body wall morphology of Pentapora foliacea (Ellis and Solander) (Bryozoa,Cheilostomata)

The ascophoran Pentapora foliacea was studied from epoxy sections of skeletal and soft (hard-soft) tissues. The basal wall is double, indicating the colony grew as two independent layers, back to back. The structure of the vertical walls and interzooidal communication organs indicates that zooids were budded in the usual way as in most encrusting cheilostomes. Secondary layers of the frontal wall are of acicular aragonite. The ovicell develops as a flattened cuticular bladder in early ontogeny; the aragonitic layer of the frontal wall later engulfs it. A median vesicle, an evagination of the vestibular wall, is present but the eggs may be supplied with sufficient yolk to nurture the embryo. The overall ovicell structure is similar to that of hyperstomial ovicells in other cheilostomes.     

Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina

Celleporella hyalina (L.) is unusual among cheilostomes in producing sexually dimorphic gonozooids which are frontally budded from a layer of sterile autozooids, and also in the possession of a placental system for extracoelomic nutrition of the developing embryo. This paper investigates these two aspects of the reproductive strategy, combining observations of living colonies with ultrastructural study of preserved material. The formation of the male and female gonozooids is described. Female zooids underwent a maximum of four successive reproductive cycles before senescence. About 29% of embryos failed to develop to completion and were prematurely expelled from the ovicell. Spermatogenesis follows the typical cheilostome pattern. Fertilization is internal, and probably occurs during vitellogenesis of the oocyte. Oogenesis involves the activity of a nurse cell. The telolecithal egg increases in volume approximately 15–fold after transfer to the ovicell, and is nourished by a relatively simple placental system formed by the distal epithelium of the maternal zooid.     

Ultrastructural evidence for nutritional exchange between brooding unionid mussels and their glochidia larvae

Abstract. The life history of unionid bivalve molluscs includes retention of developing embryos within the gills of parental mussels. This brooding behavior may facilitate nutrient transfer to the glochidia larvae, i.e., matrotrophy. To address this possibility, morphological relationships between brood chambers and developing larvae of Pyganodon cataracta and Utterbackia imbecillis were examined with TEM, and larval shells were observed with SEM, for features that could be associated with the uptake of dissolved materials. Early in brooding, glochidia are enclosed in a vitelline membrane that physically contacts numerous cilia and microvilli of the epithelial cells lining the brood chamber (marsupium). The vitelline membrane subsequently disappears. Lamellar tissues of parental mussels initially have large deposits of glycogen that diminish during the course of brooding. Septa separating brood chambers from adjacent secondary water tubes have numerous mitochondria and microvilli, suggesting the potential for active transport of materials into or out of the marsupia. Since punctae (pores) in the larval shells become filled with an organic matrix early in brooding, they are unlikely to be involved in nutrient exchange. Ultrastructure of the brood chamber and physical contact between the parental mussel and larvae are consistent with a nutritive role for retention of glochidia in the marsupia.     

Smaller amphipod mothers show stronger trade-offs between offspring size and number

Trade-offs between embryo mass and number were studied in 10 populations of the freshwater amphipod Gammarus minus . Trade-offs were stronger in populations with small brooding females than in those with larger brooding females. Relationships between embryo mass and maternal body mass were also stronger in populations dominated by small versus large brooding females. These patterns are likely the result of morphological constraints, at least in part. Embryo size is more affected by brood size and maternal size in small mothers, probably because of offspring-packaging constraints associated with small brood pouches. Energy constraints appear to be less important. These results suggest that body size may not only affect the magnitude of individual life-history traits, as is well known, but also the covariance between traits.     

Life‐history strategy,with ctenidial and pallial larval brooding,of the troglodytic ‘living fossil’ Congeria kusceri (Bivalvia: Dreissenidae) from the subterranean Dinaric Alpine karst of Croatia

Among freshwater bivalves, the brooding of embryos and larvae within the maternal ctenidia is well known. Exceptions to this generalization are the non‐brooding freshwater and estuarine species of Dreissena and Mytilopsis, respectively. It was reported that the freshwater troglodytic cousin, Congeria kusceri Bole, 1962, of these dreissenids does not brood either. It is herein demonstrated that C. kusceri undergoes one reproductive cycle each year. Sexes are separate, with an early male and later female bias. A small percentage (2.14%) of individuals is hermaphroditic. The gonads mature over summer from May to November. Spawning commences in September, when females release mature oocytes into their ctenidia and inhale sperm from mature males. Here the oocytes are fertilized, and develop within interfilamentary marsupia. Ctenidial tissues glandularize, and may provide a source of maternal nutrition for the embryos. At the late prodissoconch‐1 or prodissoconch‐2 stage (PR2, ~220 μm), larvae are released into the infrabranchial chamber via a birth channel along the outer edge of the ventral marginal food groove of both inner demibranchs. Here, they are brooded further in mantle pouches located beneath the inhalant siphon. Subsequently, after the PR2 stage (nepioconch/dissoconch), they are released from the inhalant siphon and assume an independent life as crawling juveniles. Such juveniles may be found amongst clusters of adults. Not only is C. kusceri unique amongst the Dreissenidae in possessing the capacity to brood internally fertilized ova, but it is also exceptional amongst the Bivalvia in possessing the described methods of brooding and birth. Explanations for both lie in its troglodytic lifestyle, decadal length longevity and habitat: that of byssal attachment to the hard surfaces of underground freshwater rivers, caves, pits, and sinkholes in the Tethyan arc of the Dinaric karst. Internal fertilization of a few large yolky eggs, lecithotrophic larvae, ctenidial brooding, and secondary pallial parental care represent relatively recent, Late Miocene, evolutionary adaptations from a Tethyan lentic ancestor.     

Division of labor and recurrent evolution of polymorphisms in a group of colonial animals

Rendering developmental and ecological processes into macroevolutionary events and trends has proved to be a difficult undertaking, not least because processes and outcomes occur at different scales. Here we attempt to integrate comparative analyses that bear on this problem, drawing from a system that has seldom been used in this way: the co-occurrence of alternate phenotypes within genetic individuals, and repeated evolution of distinct categories of these phenotypes. In cheilostome bryozoans, zooid polymorphs (avicularia) and some skeletal structures (several frontal shield types and brood chambers) that evolved from polymorphs have arisen convergently at different times in evolutionary history, apparently reflecting evolvability inherent in modular organization of their colonial bodies. We suggest that division of labor evident in the morphology and functional capacity of polymorphs and other structural modules likely evolved, at least in part, in response to the persistent, diffuse selective influence of predation by small motile invertebrate epibionts.     

Early Colony Development in Aetea (Bryozoa)

External structures on the erect parts of zooids of Aetea havebeen demonstrated to be brood chambers by observation of release,settlement and metamorphosis of larvae from the chambers. Theancestrula is smaller than, but very similar to succeeding zooidsin the primary zone of astogenetic change, which do not showtubular connections. Sections through brood chambers and zooidsshow that part of the brood chamber wall may be slightly calcified.Brood chambers appear to be products of the external zooid walland not diverticula derived from the tentacle sheath.