Sex, Molecules, and Gene control : Ecophysiological and evolutionary aspects of key sponge species from Antarctic shallow waters and the deep sea

Abstract: Very little is known about the ecophysiological aspects of Porifera (sponges) from Antarctica and North Atlantic, even though they are keystone components of these habitats. Being the earliest diverging metazoan lineage, sponges also play a fundamental role in our understanding of animal evolution. The main focus of this thesis was to study several aspects of the reproduction of sponges from the Antarctic shallow waters and the North Atlantic deep-sea sponge grounds and to describe the molecular toolkit that regulates their gametogenesis from an evolutionary perspective.In paper I, the reproductive strategy of six demosponge species commonly found in the shallow waters of Antarctica was examined with histological analyses. All species were brooders and although they reproduced during similar periods of the year, differences in their reproductive strategies might have allowed their coexistence in a habitat with annual food limitation events and low temperature.In paper II, the reproductive strategy of five species of the genus Geodia, a keystone genus of boreo-arctic sponge grounds, was assessed with histological analyses. All species were gonochoristic and oviparous, reproducing during similar periods (1-2 cycles annually) and with a high reproductive effort. The abundant lipid yolk and bacterial symbionts in their oocytes might enhance embryonic survival in the water column. Slight differences in reproductive strategies among species indicate specific adaptations for their successful colonization. This is the most detailed description of the reproductive biology of deep-sea Geodia sponges, providing essential information for the design of adequate conservation strategies in these vulnerable areas.In paper III, the genes and proteins regulating the oogenesis and spermatogenesis of the same five Geodia spp. were identified with RNA-seq and proteomic analyses and it was concluded that the molecular toolkit behind the main stages of gametogenesis is conserved across Metazoa. This is the most comprehensive molecular study on the gametogenesis of sponges and has profound implications for understanding the evolution of sexual reproduction in animals.In Manuscript IV, the reproductive features, the lipid signals and the accompanying gene expression patterns during oogenesis of the keystone deep-sea sponge Phakellia ventilabrum were assessed with histological, lipidomic and RNA-seq analyses. In this oviparous species, most of the triacylglycerides showed a tendency for signal increase during oogenesis, correlated with significant overexpression of genes related to their biosynthesis. This might suggest that triacylglyceride-rich yolk is the main lipid storage for the future embryo. This study unveils lipid metabolism patterns associated with female reproduction in sponges for the first time, setting the basis for a better understanding of the chemical ecology of this species and for future comparative analyses across species.