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a A succession of avicularia has been regenerated within the damaged cystids of preceding ones in Puellina venusta (Canu & Bassler, 1925). b A miniature autozooid phenotype with frontal (costal) shield, orifice, and a distal spine base has been regenerated into the cystid of an interzooidal avicularium of Puellina radiata (Moll, 1803). Soft tissue removed from these specimens
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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-occur...
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Context 1
... zooid damage is sometimes followed by regeneration of an alternate morphology. Figure 4a shows a series of adventitious avicularia that have been regenerated over time within the confines of pre- vious avicularia that were presumably damaged. In contrast, Fig. 4b shows a miniature autozooid phenotype regenerated in a like manner within the cystid of an adventitious avicularium. ...
Context 2
... frond on which a colony occurs, evidently to reduce abrasion (Xing and Qian 1999). Further, zooid damage is sometimes followed by regeneration of an alternate morphology. Figure 4a shows a series of adventitious avicularia that have been regenerated over time within the confines of pre- vious avicularia that were presumably damaged. In contrast, Fig. 4b shows a miniature autozooid phenotype regenerated in a like manner within the cystid of an adventitious avicularium. These natural experiments in regeneration reveal prospective homologies, and the possibility of regulatory 'switches' in certain zooid developmental pathways. (Canu & Bassler, 1925). b A miniature autozooid phenotype ...
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Citations
... Bryozoa is a medium-sized phylum with approximately 6700 known extant species [6] of aquatic, almost entirely colonial, filter-feeding lophotrochozoans, the vast majority of which incubate their progeny [7,8]. In addition to a large diversity of colony morphologies [9], the modular nature of colonies allows for extraordinary zooidal polymorphism [10] and associated division of labour [11], including reproduction [5,8]. Embryonic incubation is present among extant representatives of all three bryozoan classes-in all Phylactolaemata ( placental viviparity in internal embryo sacs), all Stenolaemata (intracoelomic placental viviparity with polyembryony) and most Gymnolaemata (both brooding and viviparity, sometimes placental). ...
... While Gordon & Voigt [77] agreed with the idea by Taylor [21], they also highlighted the potential importance of the origins of calcified frontal walls for the sustained increase of species numbers into the Late Eocene, including recovery from the K-Pg extinction. Also, neocheilostomes are characterized by a high degree of zooidal polymorphism, which might also have contributed to their success [11]. Furthermore, Moharrek et al. [19] found that global cheilostome genus origination rates were positively correlated with sea surface temperature. ...
Parental care is considered crucial for the enhanced survival of offspring and evolutionary success of many metazoan groups. Most bryozoans incubate their young in brood chambers or intracoelomically. Based on the drastic morphological differences in incubation chambers across members of the order Cheilostomatida (class Gymnolaemata), multiple origins of incubation were predicted in this group. This hypothesis was tested by constructing a molecular phylogeny based on mitogenome data and nuclear rRNA genes 18S and 28S with the most complete sampling of taxa with various incubation devices to date. Ancestral character estimation suggested that distinct types of brood chambers evolved at least 10 times in Cheilostomatida. In Eucratea loricata and Aetea spp. brooding evolved unambiguously from a zygotespawning ancestral state, as it probably did in Tendra zostericola, Neocheilostomata, and ‘Carbasea’ indivisa. In two further instances, brooders with different incubation chamber types, skeletal and non-skeletal, formed clades (Scruparia spp., Leiosalpinx australis) and (Catenicula corbulifera (Steginoporella spp. (Labioporella spp., Thalamoporella californica))), each also probably evolved from a zygote-spawning ancestral state. The modular nature of bryozoans probably contributed to the evolution of such a diverse array of embryonic incubation chambers, which included complex constructions made of polymorphic heterozooids, and maternal zooidal invaginations and outgrowths.
... Bryozoa is a medium-sized phylum with approximately 6700 known extant species [6] of aquatic, almost entirely colonial, filter-feeding lophotrochozoans, the vast majority of which incubate their progeny [7,8]. In addition to a large diversity of colony morphologies [9], the modular nature of colonies allows for extraordinary zooidal polymorphism [10] and associated division of labour [11], including reproduction [5,8]. Embryonic incubation is present among extant representatives of all three bryozoan classes-in all Phylactolaemata ( placental viviparity in internal embryo sacs), all Stenolaemata (intracoelomic placental viviparity with polyembryony) and most Gymnolaemata (both brooding and viviparity, sometimes placental). ...
... While Gordon & Voigt [77] agreed with the idea by Taylor [21], they also highlighted the potential importance of the origins of calcified frontal walls for the sustained increase of species numbers into the Late Eocene, including recovery from the K-Pg extinction. Also, neocheilostomes are characterized by a high degree of zooidal polymorphism, which might also have contributed to their success [11]. Furthermore, Moharrek et al. [19] found that global cheilostome genus origination rates were positively correlated with sea surface temperature. ...
Parental care is considered crucial for the enhanced survival of offspring and evolutionary success of many metazoan groups. Most bryozoans incubate their young in brood chambers or intracoelomically. Based on the drastic morphological differences in incubation chambers across members of the order Cheilostomatida (class Gymnolaemata), multiple origins of incubation were predicted in this group. This hypothesis was tested by constructing a molecular phylogeny based on mitogenome data and nuclear rRNA genes 18S and 28S with the most complete sampling of taxa with various incubation devices to date. Ancestral character estimation suggested that distinct types of brood chambers evolved at least 10 times in Cheilostomatida. In Eucratea loricata and Aetea spp. brooding evolved unambiguously from a zygote-spawning ancestral state, as it probably did in Tendra zostericola, Neocheilosto-mata, and 'Carbasea' indivisa. In two further instances, brooders with different incubation chamber types, skeletal and non-skeletal, formed clades (Scruparia spp., Leiosalpinx australis) and (Catenicula corbulifera (Steginoporella spp. (Labioporella spp., Thalamoporella californica))), each also probably evolved from a zygote-spawning ancestral state. The modular nature of bryozoans probably contributed to the evolution of such a diverse array of embryonic incubation chambers, which included complex constructions made of poly-morphic heterozooids, and maternal zooidal invaginations and outgrowths.
... Both gymnolaemates and cyclostomes have colonies with varying degrees of polymorphism, while phylactolaemates have monomorphic colonies. Polymorphic colonies include feeding autozooids and a variety of heteromorphic zooids, for example, avicularia, kenozooids, nanozooids (Cook, 1968;Hyman, 1959;Lidgard et al., 2012;Marcus, 1939;McKinney & Jackson, 1991;Mukai et al., 1997;Ryland, 1970;Schack et al., 2019;Silén, 1938Silén, , 1977. Autozooids are responsible for supplying heteromorphic zooids with nutrients, since the latter usually have a reduced polypide and are unable to feed (Carter et al., 2010;Ryland, 1970;Schack et al., 2019;Simpson et al., 2017, but see Cheetham et al., 2006;Cook, 1968). ...
Bryozoan colonies are composed of zooids, which can differ in structure and function. Autozooids supply heteromorphic zooids with nutrients, which are usually unable to feed. To date, the ultrastructure of the tissues providing nutrient transfer is almost unexplored. Here, we present a detailed description of the colonial system of integration (CSI) and the different types of pore plates in Dendrobeania fruticosa. All cells of the CSI are joined by tight junctions that isolate its lumen. The lumen of the CSI is not a single structure, but a dense network of small interstices filled with a heterogeneous matrix. In autozooids, the CSI is composed of two types of cells: elongated and stellate. Elongated cells form the central part of the CSI, including two main longitudinal cords and several main branches to the gut and pore plates. Stellate cells compose the peripheral part of the CSI, which is a delicate mesh starting from the central part and reaching various structures of autozooids. Autozooids have two tiny muscular funiculi, which start from the caecum apex and run to the basal wall. Each funiculus includes a central cord of extracellular matrix and two longitudinal muscle cells; together they are enveloped with a layer of cells. The rosette complexes of all types of pore plates in D. fruticosa display a similar cellular composition: a cincture cell and a few special cells; limiting cells are absent. Special cells have bidirectional polarity in interautozooidal and avicularian pore plates. This is probably due to the need for bidirectional transport of nutrients during degeneration-regeneration cycles. Cincture cells and epidermal cells of pore plates contain microtubules and inclusions resembling dense-cored vesicles, which are typical of neurons. Probably, cincture cells are involved in the signal transduction from one zooid to another and can be a part of the colony-wide nervous system.
... This is also a reason for the high plasticity of the growth of modular organisms capable of "filling" free space (Marfenin, 1993). The ability to resist overgrowth by neighboring epibionts and predation is also provided by the ability to secrete toxins that deter potential predators and prevent the settling and development of other epibionts (Jackson and Buss, 1975;Thacker et al., 1998), as well as the formation of protective structures, including polymorphic zooids (Cook, 1979;Winston, 1984Winston, , 1986Lidgard et al., 2012) and brood chambers Taylor, 2004, 2005;Ostrovsky et al., 2009aOstrovsky et al., , 2009bOstrovsky, 2013) (see also below). Establishment of symbiotic associations is that are broadly understood in this article as stable interactions between different species, can also contribute to the survival and successful development of organisms in the competitive environment of encrusting communities (Karlson and Shenk, 1983;Wullf, 1985; see also, Harmelin et al., 1994). ...
... In particular, a wide range of polymorphic zooids has been evolved in cheilostome bryozoans (epibionts themselves) since Cretaceous (Cheetham et al., 2006). For example, activity of some so-called avicularia presumably repells larvae of other sedentary invertebrates (Winston, 1984(Winston, , 1986Lidgard et al., 2012;Shunatova et al., 2021) (see also above). ...
The life of sedentary organisms faces strong competition for space against neighboring epibionts, and the impact of predators. The emergence of various adaptations to cope these problems includes establishing various interactions with other members of benthic communities. Various symbiotic (commensal, mutualistic, and even parasitic) relationships presented in multiple variations allow not only to succeed in the competition for free space, but also provide other equally important advantages for survival. Being one of the most abundant groups of colonial invertebrates in marine benthic ecosystems, bryozoans are not an exception. This group demonstrates both common and unique symbiotic associations. This article provides an overview of all known forms of symbiosis in Bryozoa, fossil and modern, and discusses the consequences of such relationships.
... At its most extreme, this variation within colonies is expressed as morphologically discontinuous body types, called polymorphs, which serve different functions in the colony. How polymorphism in modular animals evolves is unknown (Taylor, 2020;Lidgard et al., 2012;Simpson et al., 2017), but it is impossible to resolve without first understanding whether phenotypic distributions within colonies are actually evolvable across colony generations. To understand whether phenotypic distributions are evolvable, we turn to a clade of modular animals called bryozoans. ...
The study of trait evolution in modular animals is more complicated than that in solitary animals, because a single genotype of a modular colony can express an enormous range of phenotypic variation. Furthermore, traits can occur either at the module level or at the colony level. However, it is unclear how the traits at the colony level evolve. We test whether colony-level aggregate traits, defined as the summary statistics of a phenotypic distribution, can evolve. To quantify this evolutionary potential, we use parent-offspring pairs in two sister species of the bryozoan Stylopoma , grown and bred in a common garden breeding experiment. We find that the medians of phenotypic distributions are evolvable between generations of colonies. We also find that the structure of this evolutionary potential differs between these two species. Ancestral species align more closely with the direction of species divergence than the descendent species. This result indicates that aggregate trait evolvability can itself evolve.
... At the very least, clonal animal colonies go beyond the modularity seen in plants to add a potential level of selection to the biological hierarchy (Buss, 1987;Simpson, 2012;Simpson et al., 2020). Little-explored tradeoffs may exist between colony-and zooid-level diversification, as seen in the evolutionary differences between corals (with essentially monomorphic zooids but an extraordinary range of colony forms including solitary individuals) and bryozoans (richly polymorphic at the zooid level but lacking comparable colony sizes or diverse solitary forms) (Lidgard et al., 2012;Schack et al., 2019; at least 10 phyla have evolved polymorphic colonies, but most colonial species lack polymorphic zooids, Hiebert et al., 2021). ...
Evolvability is best addressed from a multi-level, macroevolutionary perspective through a comparative approach that tests for among-clade differences in phenotypic diversification in response to an opportunity, such as encountered after a mass extinction, entering a new adaptive zone, or entering a new geographic area. Analyzing the dynamics of clades under similar environmental conditions can (partially) factor out shared external drivers to recognize intrinsic differences in evolvability, aiming for a macroevolutionary analog of a common-garden experiment. Analyses will be most powerful when integrating neontological and paleontological data: determining differences among extant populations that can be hypothesized to generate large-scale, long-term contrasts in evolvability among clades; or observing large-scale differences among clade histories that can by hypothesized to reflect contrasts in genetics and development observed directly in extant populations. However, many comparative analyses can be informative on their own, as explored in this overview. Differences in clade-level evolvability can be visualized in diversity-disparity plots, which can quantify positive and negative departures of phenotypic productivity from stochastic expectations scaled to taxonomic diversification. Factors that evidently can promote evolvability include modularity—when selection aligns with modular structure or with morphological integration patterns; pronounced ontogenetic changes in morphology, as in allometry or multiphase life cycles; genome size; and a variety of evolutionary novelties, which can also be evaluated using macroevolutionary lags between the acquisition of a trait and phenotypic diversification, and dead-clade-walking patterns that may signal a loss of evolvability when extrinsic factors can be excluded. High speciation rates may indirectly foster phenotypic evolvability, and vice versa. Mechanisms are controversial, but clade evolvability may be higher in the Cambrian, and possibly early in the history of clades at other times; in the tropics; and, for marine organisms, in shallow-water disturbed habitats.
... Morpho-functional specialization of polymorphic modules that often lack the ability to feed and became "colonial organs" can be primitive or advanced. Nonetheless, its wide distribution among distant taxa indicates that "division of labor" independently evolved several times and "proved" its effectiveness in the evolutionary history of various lineages of colonial organisms, both benthic and nektonic Hiebert et al., 2021;Lidgard et al., 2012;Simpson et al., 2017). Zooidal polymorphism in modular living systems is thought to be a trait evolving as a result of increasing colonial integration (Beklemishev, 1969;Boardman & Cheetham, 1969, 1973Harwell, 1994;Schopf et al., 1973;Schopf 1977). ...
... It also stimulated discussion on the origins of polymorphism (e.g. Banta, 1973;Harwell, 1994;Lidgard et al., 2012;Nekliudova et al., 2021;Silén, 1938Silén, , 1977Schopf et al., 1973;Ostrovsky, 2013b). ...
... In cheilostomes, spines are presumably modified kenozooids (Silén, 1942) which have evolved to the hollow outgrowth of the zoodal wall devoid of communication pores plugged by pore-cell complexes (Ostrovsky, 1998;Martha et al., 2021). In this clade, further modification of spines (their flattening and fusion) resulted in the evolution of the protective frontal shields (Cáceres-Chamizo et al., 2017;Lidgard et al., 2012) and brood chambers (ovicells) (Ostrovsky & Taylor, 2004, 2005Ostrovsky, 2013a). In the latter, further modification of the protective capsule (ooecium) can be either accompanied by its transformation to kenozooid (Dick et al., 2021;Ostrovsky et al., 2007Ostrovsky et al., , 2009, total reduction (Ostrovsky et al., , 2009b, or reduction of its internal cavity (Ostrovsky et al., 2003(Ostrovsky et al., , 2009a. ...
Morpho-functional polymorphism of modules, also known as “division of labor”, is a widespread phenomenon independently evolving multiple times in the colonies of many aquatic invertebrates and invertebrate chordates. Polymorphic zooids are especially diverse among Cheilostomata, the evolutionarily most successful clade in the phylum Bryozoa. The most diverse among cheilostome polymorphs are avicularia and vibracularia, acting as defensive, repelling, cleaning and locomotory “colonial organs”. While their skeletal characters were intensively studied, the soft tissues have largely been neglected. This hampers evolutionary interpretations. In this study, we compared the muscular system in five contrasting types of these polymorphs from 10 species of eight related as well as distant families. In contrast with the prevailing view, we found that the structural and functional changes affecting the muscular system during evolutionary transition from autozooid to polymorph were considerably more diverse and complex than mere “vestigialization”. These changes included muscle loss, hypertrophy, rearrangement (regrouping and relocation), fusion, and acquisition of asymmetry and muscle striation. Asynchronous contraction of originally synchronously working muscles was presumably evolved in advanced vibracularia. Some of these modifications were recorded in all avicularian types, whereas others were characteristic only for particular taxa or polymorphic categories. Our study showed that not only skeletal, but also soft parts of the polymorphs were evolutionarily very flexible and modified to various degrees and in various directions.
... The term polyphenism is used instead when development toward one or the other form can be attributed to external influences and, therefore, takes place in the absence of genetic differences (i.e., phenotypic plasticity [12][13][14]). However, precise information on the mechanisms involved is generally lacking [15]; moreover, the divide between polymorphism and polyphenism can be very thin [16]. We should therefore have a flexible approach while collecting classes of phenomena that traditionally would be considered as separate due to the parameters used to describe them. ...
Irrespective of the heuristic value of interpretations of developmental processes in terms of gene regulatory networks (GRNs), larger-angle views often suffer from: (i) an inadequate understanding of the relationship between genotype and phenotype; (ii) a predominantly zoocentric vision; and (iii) overconfidence in a putatively hierarchical organization of animal body plans. Here, we constructively criticize these assumptions. First, developmental biology is pervaded by adultocentrism, but development is not necessarily egg to adult. Second, during development, many unicells undergo transcriptomic profile transitions that are comparable to those recorded in pluricellular organisms; thus, their study should not be neglected from the GRN perspective. Third, the putatively hierarchical nature of the animal body is mirrored in the GRN logic, but in relating genotype to phenotype, independent assessments of the dynamics of the regulatory machinery and the animal’s architecture are required, better served by a combinatorial than by a hierarchical approach. The trade-offs between spatial and temporal aspects of regulation, as well as their evolutionary consequences, are also discussed. Multicellularity may derive from a unicell’s sequential phenotypes turned into different but coexisting, spatially arranged cell types. In turn, polyphenism may have been a crucial mechanism involved in the origin of complex life cycles.
... Cheilostome bryozoans have exceptionally useful traits for tackling some long-standing questions in evolutionary biology. Such traits include a calcified skeleton that renders these marine organisms very fossilizable (7), external, calcified brooding structures that allow fecundity (a fitness component) to be quantified in the fossil record (15), a colonial and modular nature that allows the estimation of sources of phenotypic variation among and within individual genotypes and environments (26,27), polymorphic structures that represent ergonomically partitioned divisions of labor (28,29), and ecological interactions "frozen in time" (6,14). Analyzing molecular sequence data, independent of morphological traits used to identify species, to infer evolutionary relationships, we lend strong support to important assumptions often invoked in the cheilostome literature with limited empirical support. ...
... Models of speciation and extinction rates of nonbrooding and brooding cheilostomes are compared using the Akaike criteria. The italicized model (cid2, a character-independent model that is the null version of a BiSSE model) has the AIC highest model weight in this set of models, followed closely by a more complex character-independent model (cid4 the original ones (29). A diversity of traits, derived from polymorphs in a modular construction, which permit varied or even novel ecological function, could allow the occupation of new niches and thus promote macroevolutionary diversification (28). ...
Phylogenetic relationships and the timing of evolutionary events are essential for understanding evolution on longer time scales. Cheilostome bryozoans are a group of ubiquitous, species-rich, marine colonial organisms with an excellent fossil record but lack phylogenetic relationships inferred from molecular data. We present genome-skimmed data for 395 cheilostomes and combine these with 315 published sequences to infer relationships and the timing of key events among c. 500 cheilostome species. We find that named cheilostome genera and species are phylogenetically coherent, rendering fossil or contemporary specimens readily delimited using only skeletal morphology. Our phylogeny shows that parental care in the form of brooding evolved several times independently but was never lost in cheilostomes. Our fossil calibration, robust to varied assumptions, indicates that the cheilostome lineage and parental care therein could have Paleozoic origins, much older than the first known fossil record of cheilostomes in the Late Jurassic.
... Bryozoan colonies consist of a number of individuals, called "autozooids" which perform asexual reproduction (budding) to multiply their colony members [70]. In addition to these autozooids, some bryozoan species (especially species belonging to the order Cheilostomata) possess specialized individuals, such as sexually dimorphic zooids, brooding zooids, structural zooids and defensive zooids [71,72]. Among those, "avicularia" is a type of defensive zooids, since, in some species, they look like avian heads with biting mandibles [72]. ...
Most animal species spend their lives in a form based on the unit of “an individual” that is a sophisticated multicellular closed unit with various biological functions. Although the system of an animal individual seems to be perfect, individuals belonging to some animal lineages constitute higher-dimensional units, i.e., colonies, that consist of multiple individuals of the same species, performing divisions of labors among them. Those animals include eusocial insects and colonial animals, and their colonies are also known as “superorganisms”, since a colony behave as a single individual. Recent molecular and genomic/transcriptomic studies have been revealing the regulatory mechanisms underlying the integrated systems of superorganisms although many aspects have yet to be elucidated. In this article, life patterns of superorganisms in some animals are introduced, together with recent research advances on the mechanisms. Furthermore, animal species that show distinctive developmental systems such as abnormal asexual reproduction are also focused, since those developmental patterns are deviated from the concept of normal animal “individuality”. Furthermore, synthetic approaches based on robotics and mathematical modeling, focusing on novel robotic systems that can self-organize various non-trivial macroscopic functionalities as observed in superorganisms, are also discussed.
