Evolution of matrotrophy and placental analogues in Bryozoa

The phylum Bryozoa, all species of which are aquatic colonial suspension feeders, is unique among invertebrates in possessing matrotrophy in all major classes. Extraembryonic nutrition is thought to have evolved numerous times in Bryozoa, thus making them an extraordinary model for the study of convergent evolution. The proposed project will focus on comparative anatomical and ultrastructural analysis of nourishing organs in both marine and freshwater Bryozoa aiming to reconstruct the major stages and to reveal the major trends in the evolution of matrotrophy, and to follow a pattern of distribution of the reproductive modes throughout the phylum. A new hypothesis concerning the origin of incipient matrotrophy followed by the shift in oogenesis will be tested by comparing the epithelial lining of the brood chambers and oogenesis mode in a number of species from different families. The idea on the increasing complexity of the nutritional adaptations and the transition from absorbotrophic nutrition to nourishment via placental analogues throughout the phylum will be tested too. In particular the focus will be on the structural complexity and intimacy of the contact between maternal and embryonic tissues, and cytological mechanisms providing transfer of substances at the different stages of incubation in the brood chambers of different types. Ultrastructural interconnections with symbiotic bacteria, developing in the funicular tissue of some matrotrophic bryozoans will be investigated. This part of the project will also focus on the search for `new` matrotrophic species possessing symbionts, thereby providing perspectives for current studies on bryostatins - secondary metabolites with high medical potential. Cytological structures will be investigated using light- and transmission electron microscopy and 3D computer reconstruction. In addition to its broad relevance to the field of reproductive biology and evolution of reproductive modes in clonal sessile organisms, the proposed research will provide an essential contribution to the further understanding of convergent evolution of parental care in eumetazoans, and, particularly, evolution of extraembryonic nutrition in invertebrates. In summary, the project will integrate the morphological, functional and symbiotic aspects of bryozoan matrotrophy aiming to reveal the major patterns of its evolutionary trajectory.

In the great majority of sexual organisms, mothers reproduce by laying eggs that develop and hatch in the outer environment. Matrotrophy (or extraembryonic nutrition) direct transfer of nutrients from mother to embryo during gestation is the exception among animals. It is most familiar to us in a particular form, placentation, which humans share with other mammals. Matrotrophy is best known and thoroughly studied among vertebrates, but until now, its occurrence and distribution among invertebrates was at best haphazardly documented, scattered across disparate studies in specialist literature. Moreover, the general opinion is that only a few invertebrates possess this sophisticated kind of parental care. I therefore believe that my comprehensive study of matrotrophy across the fully colonial aquatic phylum Bryozoa is important and in some ways astonishing. Exceeding all previous studies, my results show occurrence of matrotrophy in 39 genera of 26 families of the bryozoan class Gymnolaemata. Species belonging to the classes Stenolaemata and Phylactolaemata are all matrotrophic. Thus, the phylum Bryozoa includes more matrotrophic species than in any other aquatic invertebrate phylum.My project focused on comparative anatomical and ultrastructural analysis of nourishing organs and oogenesis in both marine and freshwater Bryozoa, aiming to reconstruct the major stages and to reveal the major trends in the evolution of matrotrophy. By following a distribution pattern of the reproductive modes throughout the phylum, the evidence for multiple independent origins of placental analogues was obtained. A new hypothesis concerning the origin of incipient matrotrophy followed by the shift in oogenesis was successfully tested. In the course of the project the first anatomical description of incipient placentotrophy in invertebrates has been made. Thecombinations of contrasting oocytic types (macrolecithal or oligolecithal) and various degrees of placental development and embryonic enlargement during incubation, found in different bryozoan species, are suggestive of a transitional series from the incipient to the substantial placentotrophy accompanied by an inverse change in oogenesis, a situation reminiscent of some vertebrates. The results of this study show that this phylum, with its wide variety of reproductive patterns, incubation devices and types of the simple placenta-like systems, offers a promising model for studying parallel evolution of placentotrophy in particular, and matrotrophy in general.