The Ecology of Freshwater Planarians

Abstract

Planarians are on the rise as a model system for regeneration and stem cell dynamics. Almost in parallel the interest in planarian field biology has declined. Besides representing an independent research discipline in its own right, understanding of the natural habitat is also directly relevant to optimizing culture conditions in the laboratory. Moreover, the current laboratory models are but few of hundreds of planarian species worldwide. Their adaptation to a wide range of ecological niches has resulted in a fascinating diversity of regenerative abilities, body size, reproduction strategies, and life expectancy, to name just a few. With the currently ongoing establishment of large planarian species collections, such phenotypic diversity becomes accessible to comparative mechanistic analysis in the laboratory. Overall, we hope that this chapter inspires an integral view of the planarian model system that not only includes the molecular and cellular processes under investigation but also the evolutionary forces that shaped them in the first place.

Why isn’t sex optional? Stem-cell competition, loss of regenerative capacity, and cancer in metazoan evolution

“…While the sexualization mechanism in this case remains unknown, up-regulation of canonical Wnt pathway activity has been shown to both suppress regeneration and sexualize in other planarian species (Sikes and Newmark, 2013;Sureda-Gómez, Martín-Durán and Adell, 2016). On the basis of these results, Vila-Farré and Rink (2018) have suggested that Wnt pathway activity, which is known to be essential for the regeneration of posterior structures in planaria, may also serve as a switch between gametic and vegetative reproduction. As Wnt is a versatile, early-as well as late-acting regulator of both polarity and cell fate across multicellular animals, confirmation of a mechanistic link between Wnt activity, regeneration, and sexualization outside of the planaria would provide broader evidence for the competitive model proposed here.…”

“…If non-germline stem cells "win" and suppress germline development, obligate vegetative asexuals that altogether lack specialized germline stem cells, gametes, or gonads, such as the laboratory model planaria Dugesia japonica or Schmidtea mediterranea can be expected. Population variants or close relatives of both of these species are sexual, suggesting that full suppression of germline development is not stable over evolutionary timescales (Sluys and Riutort, 2018;Vila-Farré and Rink, 2018). If, on the other hand, germline stem cells "win" and suppress totipotency in non-germline stem cells, obligate gametic reproducers incapable of WBR can be expected.…”

“…Cooperation enables sex and hence a new genotype for which lethality is lower, and the cycle repeats itself. Such cyclic sexuality occurs in planaria (Sluys and Riutort, 2018;Vila-Farré and Rink, 2018), though single populations that alternate between sexual and asexual (vegetative) reproduction appear to be rare. Fig.…”

“…For many animals, sex is optional. Placozoa (Miller and Ball, 2005), sponges (Ereskovsky, Renard and Borchiellini, 2013), ctenophores (Martindale, 2016), cnidarians (Fautin, 2002), basal bilaterians including acoels (Bouriat and Hejnol, 2009), various invertebrates including flatworms (Rink, 2018) and annelids (Zattara and Bely, 2016), and even basal chordates, the colonial ascidians (Kürn et al, 2011) provide examples of vegetative (i.e. agametic) reproduction by budding, fission, or fragmentation accompanied by whole-body regeneration (WBR) in species that are also sexually competent (see Slack, 2017;Lai and Aboobaker, 2018;Subramoniam, 2018 for comparative analysis).…”

“…As Lai and Aboobaker (2018) point out, WBR strongly correlates with the presence of non-germline stem cells expressing components of the hypothesized germline multipotency program (GMP; Juliano, Swartz and Wessel, 2010), including the PIWI/piRNA transposon repression system (Ross, Weiner and Lin, 2014;Czech et al, 2018), vasa (Gustafson and Wessel, 2010), nanos (De Keuckelaere et al, 2018), tudor (Pek, Anand and Kai, 2012), and other typically germline regulators. At least in flatworms (Sluys and Riutort, 2018) and annelids (Zattara and Bely, 2016), vegetative reproduction also requires specific behaviors (e.g. to induce fission) that can be lost separately.…”