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Viable populations of the cheilostome bryozoan Cribrilina mutabilis Ito, Onishi & Dick exist in the NW Pacific (Russian Far East and northern Japan), NE Atlantic (Scandinavia and Scotland), and NW Atlantic (Maine, USA). The first NE and NW Atlantic records are from Norway (2008) and Casco Bay, Maine, USA (2018), respectively, indicating a relatively recent introduction to the region. Mitochondrial COI gene sequences from North Atlantic populations (Sweden, Norway, and Maine) showed two haplotypes differing by one substitution, but differed from two haplotypes from Akkeshi, northern Japan, by 6-8 substitutions. North Atlantic populations differed morphologically from the Akkeshi population in that some zooids formed a suboral projection, and frontal zooids were more common. While C. mutabilis in northern Japan has been found only on natural or artificial eelgrass ( Zostera marina ), across its range it has been found on several species of algae, plastic panels and strips, several species of Zostera , and mollusc shells. Similar frequencies of heteromorphic zooids with differing degree of frontal wall calcification, i.e., R (rib)-, I (intermediate)-, and S (shield)-type zooids, in colonies on eelgrass at comparable times of the season and across populations suggest an innate response to seasonal environmental fluctuations, although zooid frequencies were different on non-eelgrass substrates. The increase in trans-Arctic shipping along the Northern Sea Route in recent decades, and previous documentation of C. mutabilis on ship hulls in the Sea of Japan, indicate a clear mechanism for anthropogenic introduction from the Far East to Europe in recent decades.

Polyembryony-the production of multiple cloned embryos from a single fertilised egg-is a seemingly paradoxical combination of reproductive modes that nevertheless persists in diverse taxa. We document features of polyembryony in the Cyclostomata (Bryozoa)-an ancient order of modular colonial marine invertebrates-that suggest a substantial reduction in the paradoxical nature of this enigmatic reproductive mode. Firstly, we provide molecular evidence for polyembryony in three exemplar species, supporting the widely cited inference that polyembryony characterises the entire order. Secondly, genotyping demonstrates protracted release of cloned offspring from the primary embryo in a given gonozooid (chamber for embryonic incubation), thus exposing the same genotype to changing environmental conditions over time. Finally, we confirm that each gonozooid produces a distinct genotype, with each primary embryo being the result of a separate fertilisation event. We hypothesise that the sustained release of one or a few genotypes against varying environmental conditions achieves levels of risk-spreading similar to those in organisms that release multiple, unique genotypes at a single time. We argue that polyembryony, specifically with the production of a large number of progeny per fertilisation event, has been favoured in the Cyclostomata over long geological periods., Competing Interests: The authors have declared that no competing interests exist.

Prolific polyembryony is reported in few major taxa, but its occurrence has generated theoretical debate on potential conflict between sexual and asexual reproduction. It is, therefore, important to genetically confirm a widely cited inference, based on microscopy, that polyembryony characterizes marine bryozoans of the order Cyclostomata. Microsatellite genotyping of brooded embryos and maternal colonies conclusively demonstrated polyembryony, while genetic variation among broods within colonies indicated outcrossing via water-borne sperm, in the rocky-shore species Crisia denticulata. The characteristically voluminous brood chamber of cyclostomes is judged to be an adaptation linked to larval cloning and hence an indicator of polyembryony. We speculate that although the almost universal occurrence of polyembryony among crown-group Cyclostomata is probably attributable to phylogenetic constraint, adaptive consequences are likely to be significant.

We estimated fusion frequency with respect to coancestry in the bryozoan Celleporella hyalina, whose briefly planktonic sexually produced larvae settle on algal substrata and proceed to form encrusting colonies by iterative budding. Frequency of fusion between paired colonies growing on an artificial substratum was positively correlated with coefficient of relatedness, with allorecognition ability increasing during the early stages of colonial growth after larval settlement. Parents repressed the growth of F1 progeny with which they had fused. The results are concordant with the Feldgarden-Yund model of selection for self-recognition, which regards fusion with kin as an inevitable source of error whose cost diminishes with increasing relatedness. Contrary to fusion compatibility, gametic compatibility is negatively correlated with coancestry, indicating a need for further research on the possibility of common or linked genetic control that has opposite effect at somatic and gametic levels.

Fertilization success may be severely limited in marine invertebrates that spawn both male and female gametes. In a diverse group of aquatic organisms only sperm are released, with sperm-egg fusion occurring at the mother. Here, we report fertilization kinetics data for two such 'brooding' or 'spermcast' species--representing each major clade of the animal kingdom. High levels of fertilization were achieved at sperm concentrations of two or three orders of magnitude lower than is common with broadcast spawning species. At a concentration of 100 sperm ml(-1), fertilization rates of a bryozoan and colonial ascidian were near maximum, whereas most broadcast spawners would have displayed near complete reproductive failure. A further experiment looked at the rate of uptake of sperm under natural conditions. Results suggested that sperm released at ca. 0.9 m from an acting female could be collected at a rate of 3-12 times greater than the minimum required simply to avoid sperm limitation. Thus, evolutionary pressures on gametic and other reproductive characteristics of many species that release sperm but retain eggs may be quite different from those of broadcast spawners and may confer on the former an enhanced scope for sperm competition and female choice.

Sex-allocation theory developed for hermaphroditic plants predicts that impaired phenotype or reduced parental survivorship caused by environmental stress should induce relatively greater allocation to the male function. We provide experimental evidence of stress-induced maleness, already well documented in flowering plants, in a modular animal. By using cloned copies of replicate genotypes, we show that the marine bryozoan Celleporella hyalina increases the ratio of male to female modules in response to diverse environmental stressors. Mating trials confirmed that paternity is determined by fair-raffle sperm competition, which should obviate local mate competition at characteristic population density and promote the advantage of increased male allocation. The demonstrated similarity to plants transcends specific physiological pathways and suggests that stress-induced bias toward male function is a general response of hermaphroditic modular organisms to impaired prospects for parental productivity or survival.

Young colonies of the bryozoan Celleporella hyalina are capable of acquiring water-borne allosperm and of using it to fertilize ova for a period of 3-6 weeks after reaching female sexual maturity. In these simultaneous hermaphrodites, early allocation to female modules, but not male, is greatly enhanced by the acquisition of allosperm. The degree of enhancement is inversely proportional to coancestry of the recipient and donor colonies, thus promoting outcrossing. This apparently novel mechanism of adjusting operational sex ratio depends on the uptake and storage of sperm by nonreproductive (somatic) modules and subsequent translocation to females.

A diverse array of sessile marine invertebrates mate by passive dispersal of sperm which fertilize the brooded eggs of neighbours. In two such species, a sea-mat (phylum Bryozoa) and an ascidian (phylum Chordata), vitellogenic egg growth is absent in reproductively isolated specimens, but is triggered by a water-borne factor released by conspecifics. In both of these colonial, hermaphroditic species, the active factor can be removed from water by filtration. The effect involves self-/non-self-recognition: water conditioned by a separate subcolony of the same genetic individual does not prompt oocyte growth. In each species, allosperm move from the surrounding water to the ovary and are then stored in close association with the growing oocytes. We concluded that sperm themselves are the water-borne factor that triggers the major phase of female reproductive investment. This mechanism is, to our knowledge, previously undescribed in animals, but has parallels with the initiation of maternal investment in flowering plants following the receipt of compatible pollen. The species studied may be representative of many other aquatic invertebrates which mate in a similar way. The stimulation of egg growth by allosperm could lead to intersexual conflict during oogenesis.