Prudent female allocation by modular hermaphrodites: female investment is promoted by the opportunity to outcross in cyclostome bryozoans

Abstract

Many sessile, suspension-feeding marine invertebrates mate by spermcasting: aquatic sperm are spawned and gathered by conspecific individuals to fertilize eggs that are generally retained during development. In two phylogenetically distant examples, a cheilostome bryozoan and an aplousobranch ascidian, the receipt of allosperm has previously been shown to alter sex allocation by triggering female investment in eggs and brooding. Here we report experiments demonstrating that two species of cyclostome bryozoan also show restrained female investment in the absence of mating opportunity. In Tubulipora plumosa, the production of female zooids and progeny is much reduced in reproductive isolation. In Filicrisia geniculata, development of distinctive female zooids (gonozooids) begins but halts in the absence of mating opportunity, and no completed gonozooids or progeny result. Reduced female investment in the absence of a mate thus occurs in at least two orders of Bryozoa, but significant differences in detail exist and the evolutionary history within the phylum of the mechanism(s) by which female investment is initiated might be complex. The broadening taxonomic spectrum of examples where female investment appears restrained until allosperm becomes available may signify a general adaptive strategy among outcrossing modular animals, analogous to similarly adaptive sex allocation typical of many flowering plants.

Colonies as dynamic systems: reconstructing the life history of Cribrilina annulata (Bryozoa) on two algal substrates

“…With one possible exception ( Filicrisia geniculata , see Jenkins et al ., 2015), bryozoans have monoecious colonies consisting of sterile and sexual zooids, either gonochoristic or hermaphroditic that could be protandrous, protogynous or simultaneous hermaphrodites (Reed, 1991; Ostrovsky, 2013). Thus, initially sterile, a colony could continue as male, female or hermaphrodite.…”

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

“…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, ). The high cost of brooding may limit the number of gonozooids present in a colony (Hughes et al, ; Jenkins et al, ), and species of cyclostomes reduce female investment in the absence of alien sperm.…”

“…Therefore, the gonozooid and embryonic multiplication and growth must be supported via resource transfer from autozooids (Jenkins, Bishop & Hughes, ). The high cost of brooding may limit the number of gonozooids present in a colony (Hughes et al, ; Jenkins et al, ), and species of cyclostomes reduce female investment in the absence of alien sperm. When reproductively isolated, Tubulipora plumosa reduced both gonozooid production and the number of larvae (produced through intraclonal self‐fertilization), while female Filicrisia geniculata formed incomplete gonozooids (Jenkins et al, ).…”

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

“…1 , 2 ). Except for one known example, cyclostomes are colonial hermaphrodites with either zooidal gonochory or hermaphroditism and pronounced sexual zooidal polymorphism [ 16 , 20 , 36 , 69 ]. Sperm is produced in autozooids, whereas female zooids (either autozooids or autozooidal polymorphs possessing a polypide—a tentacle crown associated with a gut) form an ovary, degenerate their polypide and become gonozooids.…”