Asexual and puzzling sexual reproduction of the Mediterranean sponge Haliclona fulva (Demospongiae): life cycle and cytological structures

Abstract

Despite the common assumption that most Haplosclerida are viviparous sponges, this study of the reproductive cycle of Haliclona fulva demonstrates that this species is actually oviparous and gonochoric. Intriguingly, not a single male was recorded in 15 months of sampling. Oogenesis is synchronous, starting in late April and terminating in September. Asexual reproduction is represented by cyclic budding, which occurs from late November to early March. During the season of asexual reproduction, the reproductive effort represents from 0.21% to 1.49% of the parental tissue, with the highest values being recorded in winter. During the season of sexual reproduction, the female reproductive effort ranges 0.05–1.15%, with the highest effort appearing in early summer. However, no significant correlation between reproductive efforts and seawater temperature fluctuations could be detected. We describe the ultrastructural morphogenesis of the buds for the first time in this species. This process is asynchronous, with buds of variable size being attached to the maternal apical surface via a short stalk. Young buds lack any particular anatomical organization, whereas bud maturity is characterized by the development of mesohyl and by the appearance of an increasing number and volume of lacunae in the central part of each bud. At this stage, buds harbor numerous small choanocyte chambers scattered throughout the inner region, and all cell types known from the mesohyl of parental sponges: microgranular cells, granular cells, archaeocytes, endopinacocytes and exopinacocytes, central cells, and sclerocytes.

Metabolome variability for two Mediterranean sponge species of the genus Haliclona: specificity, time, and space

“…The significant decrease in the specialized metabolites of both species is in accordance with the ODT theory, indicating an investment towards the start of the sexual reproduction cycle. For both H. fulva and H. mucosa, this shift occurs only at the early stages of sexual reproduction when the animal needs to trigger the development of sexual gametes, and not throughout all the gametogenesis process, which in H. fulva lasts until September (Ereskovsky et al 2017). Tradeoff between the production of specialized metabolites and reproduction has been previously reported in the homoscleromorph sponge Oscarella balibaloi, however in this case it was observed at the peak of the reproductive effort (Ivanisevic et al 2011).…”

“…fulva has been recently characterised, and a shift from asexual to sexual reproduction has been reported in early April (Ereskovsky et al 2017). We therefore hypothesize that this reproduction shift induces a change in the metabolite content as reflected for both sponges metabolomes in April and May.…”

­Reproductive strategies of two common sympatric Mediterranean sponges:Dysidea avara(Dictyoceratida) andPhorbas tenacior(Poecilosclerida)

“…Long spermatogenesis periods, spanning several months, have been reported in tropical sponges ( Ettinger-Epstein et al, 2007 ; Whalan, Battershill & De Nys, 2007 ; Abdul Wahab, De Nys & Whalan, 2012 ), likely with repeated short sperm release events ( Ilan, 1995 ). However, spermatogenesis is generally completed in a short time in temperate sponges ( Scalera-Liaci, Sciscioli & Materrese, 1973 ; Corriero et al, 1998 ; Lepore et al, 2000 ; Riesgo & Maldonado, 2008 ; Piscitelli et al, 2011 ; Ereskovsky, Geronimo & Perez, 2017 ). A single short period of spermatogenesis can explain why we detected male structures only in two sampling months (June 2009 and August 2010) in P. tenacior and none in D. avara .…”

In Search of the Ancestral Organization and Phylotypic Stage of Porifera

“…General characteristics of the buds formed in all sponges except Oscarella (Homoscleromorpha) (Ere-skovsky and Tokina, 2007) appear during the initial stages of development, when they look like a dense conglomerate of different cell types at the parent sponge surface. Such buds have neither canals nor an osculum, and only very rare choanocyte chambers (for review see: Fell, 1993;Ereskovsky et al, 2017). After detachment from parent body, buds settle on the substrate, attach to it and begin the formation of the aquiferous system and growth.…”