Phylogenetically Widespread Polyembryony in Cyclostome Bryozoans and the Protracted Asynchronous Release of Clonal Brood-Mates

Abstract

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.

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

“…Stenolaemates acquired matrotrophic viviparity inside enlarged gonozooids that could have triggered the evolution of polyembryony (Ostrovsky, 2013 a , b ). Despite the paradoxical nature of releasing genetically identical embryos (Ryland, ; Craig et al ., ; Hughes et al ., ; Jenkins et al ., ) this reproductive pattern appears successful and may be correlated with the Mesozoic radiation of Cyclostomata.…”

“…As far as is known, all cyclostomes possess polyembryony, i.e. a fertilized egg gives rise to the primary embryo that buds more than a hundred larvae (Harmer, , , ; Robertson, ; Borg, ; Jenkins et al ., ; U. A. Nekliudova, T. F. Schwaha & A. N. Ostrovsky, unpublished data).…”

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

“…Although the vast majority of bryozoans are colonial hermaphrodites, there may be dioecious cyclostome colonies composed of only male autozooids or sterile autozooids, female autozooids (future gonozooids) and gonozooids, which are incapable of self‐fertilization [e.g. Filicrisia geniculata (Jenkins et al, )]. The sex ratio within colonies can also be influenced by environmental conditions: when exposed to stress the cheilostome Celleporella hyalina increased production of males and suppressed investment in brooding females (Hughes et al, ).…”

“…Lecithotrophic larvae (Ström, ) are released from the gonozooid via the ooeciostome, which is curved to direct larvae away from the feeding currents of autozooids (Schäfer, ). Larvae are released over an extended period (≤69 days in Filicrisia geniculata ), suggesting prolonged budding of the primary embryo (Jenkins et al, ).…”

“…Gonozooids are expensive to maintain. It is unlikely that a single degenerated polypide could provide sufficient nutrients for the development of over 150 larvae (Kluge, 1962, in Jenkins et al, ) during an extended period. Therefore, the gonozooid and embryonic multiplication and growth must be supported via resource transfer from autozooids (Jenkins, Bishop & Hughes, ).…”