The Role of Stem Cell Strategies in Coping with Environmental Stress and Choosing Between Alternative Reproductive Modes: Turbellaria Rely on a Single Cell Type to Maintain ­Individual Life and Propagate Species

Abstract

Abstract. To contribute to a better understanding of the interrelationships of different forms of asexual and sexual reproduction in the Turbellaria, three selected species were studied with respect to the cellular correlates underlying the diverse reproductive strategies. The exclusively asexual freshwater triclad Dugesia tahitiensis holds the top position in regenerative and fissioning capacities within the Tricladida and, in addition, has the most neoblasts (stem or regenerative cells) known within this taxon. A reproductive rate of roughly one new specimen originating from a parent animal every third day at optimal experimental conditions correlated well with the speed of head regeneration ranging from 43 to 59 h at 23 °C. The process of fission (architomy) was observed and its dependence on population density and melatonin content was studied. In two new marine representatives of the Macrostomorpha from the Adriatic Sea, the distribution of neoblasts in the body and their fate during regeneration were traced by a recently developed labelling method with 5‐bromo‐2’‐deoxyuridine. In Macrostomum, a sexual species with poor regenerative potential, the proliferating cells were localized predominantly along the nerve cords and migrated to their final location after mitosis. Microstomum n. sp., with asexual reproduction, showed a less concentrated pattern of proliferating stem cells, being localized in the future areas of organ primordia forming before fission in the process of paratomy. The findings are discussed with respect to cell biological, ecological and evolutionary implications.

Pluripotent Gametogenic Stem Cells of Asexually Reproducing Invertebrates

“…Funayama believes that both archaeocytes and choanocytes of sponges are pluripotent. Neoblasts of planarians are considered totipotent (Shibata et al, 1999;Gschwentner et al, 2001;Peter et al, 2001;Sköld et al, 2009) or pluripotent (Shibata et al, 2010). Similarly, stem cells of colonial rhizocephalan crustaceans can also be considered totipotent (Isaeva et al, , 2008b(Isaeva et al, , 2009Shukalyuk et al, , 2007 or pluripotent.…”

“…Interstitial cells in hydra and other cnidarians can produce both germline cells and some but not all somatic cell types, since epidermal and gastrodermal cells are also capable of mitotic reproduction; so the stem cell system in hydroids includes interstitial, epidermal and gastrodermal stem cells continuously undergoing the mitotic cycle (Campbell, 1974;Thomas & Edwards, 1991;Bode, 1996). For the identification of stem cells capable of mitotic reproduction, bromodeoxyuridine, a thymidine analogue, was successfully used to reveal DNA synthesis in interstitial cells in hydra (Teragawa & Bode, 1990), and neoblasts in flatworms (Gschwentner et al, 2001;Peter et al, 2001). Ethynyl deoxyurudine, another thymidine analogue, was employed for the same purpose in the ctenophore Pleurobrachia pileus (Alié et al, 2011).…”

“…The ability to differentiate into gametogenic and somatic cells was shown for archaeocytes and choanocytes in sponges (Simpson, 1984;Müller, 2006;Funayama, 2008;Funayama et al, 2010), interstitial cells in hydra and other cnidarians (Thomas & Edwards, 1991;Bode, 1996;, turbellarian neoblasts (Shibata et al, 1999;Peter et al, 2001;Isaeva et al, 2005), stem cells of colonial rhizocephalans , ascidian stem cells (Pancer et al, 1995;Stoner & Weissman, 1996;Stoner et al, 1999;Weissman, 2000). So, pluripotent stem cells in invertebrates with asexual reproduction are potentially gametogenic cells.…”

“…The gonial cells and early oocytes developing from interstitial cells are distinct from them only by a greater size (Thomas & Edwards, 1991). Gametogenic potentiality was most convincingly displayed using planarians (Baguña et al, 1989;Peter et al, 2001;Shibata et al, 1999). Neoblasts of asexually reproducing planarians and other Turbellaria are able to differentiate into germ and somatic cells of all types (Agata & Watanabe, 1999;Shibata et al, 1999;Peter et al, 2001;Orii et al, 2005).…”

“…Gametogenic potentiality was most convincingly displayed using planarians (Baguña et al, 1989;Peter et al, 2001;Shibata et al, 1999). Neoblasts of asexually reproducing planarians and other Turbellaria are able to differentiate into germ and somatic cells of all types (Agata & Watanabe, 1999;Shibata et al, 1999;Peter et al, 2001;Orii et al, 2005). According to our data, neoblasts can become gonial cells: among individuals in asexual race of Girardia tigrina that reproduced exclusively by architomy during 40 years, one planaria laid cocoons after spontaneous sexualization; histological and ultrastructural study of this planaria demonstrated the presence of gonads, gonial cells, and oocytes .…”