Platyhelminthes (Flatworms)

Platyhelminthes is a diverse group of dorsoventrally flat bilaterians with complicated life history strategies and unusual morphologies in parasitic species (Hyman 1951b).

Flatworms also have segmental traits of different kinds and degrees, such as an orthogonal nervous system or the proglottids in tapeworms.

In free-living flatworms, the longitudinal nerve cords—which vary from a single pair to multiple pairs—are intercepted by ladder-like transverse commissures forming an orthogonal grid pattern historically referred to as the orthogon (Figure 9.31) (Reisinger 1925; Reuter and Gustafsson 1995; Halton and Gustafsson 1996; Reuter, Mantyla, and Gustafsson 1998). The arrangement was initially identified in classical platyhelminth works (e.g., Lang 1881; Wheeler 1894; Wilhelmi 1909), but as more species were analyzed, a whole range of variation within the orthogon basic pattern was revealed, from dense and regular to sparse and uneven grids (Reuter and Gustafsson 1995; Reuter, Mantyla, and Gustafsson 1998). Notably, the arrangement is also absent in planktonic larval stages (Rawlinson 2010).

The orthogon is formed during embryonic development with the longitudinal nerve cords usually developing first, and the transverse commissures appearing later (Younossi-Hartenstein, Jones, and Hartenstein 2001; Cardona, Hartenstein, and Romero 2005; Monjo and Romero 2015). However, it remains unclear if these commissures are formed progressively from anterior to posterior, and which cellular processes involved. One hypothesis is that neurons migrate from the brain while the longitudinal connectives are extending, and periodically settle to form the transverse projections. A second possibility is that totipotent stem cells present in the mesenchyme (i.e., neoblasts) differentiate into neurons at regularly spaced loci, perhaps guided by the longitudinal nerve cords, to produce the commissures (Younossi- Hartenstein, Jones, and Hartenstein 2001). The latter—also known as “interstitial neural progenitor mode” (Hartenstein and Stollewerk 2015)—has been shown to occur during the regeneration of the planarian nervous system (e.g., Nishimura et al. 2011), but both mechanisms likely play a role in the patterning of these commissures.

Another featured trait of flatworms is the lattice-like musculature with serially arranged circular muscles (Figure 9.3J) (Rieger et al. 1991, 1994; Reiter et al. 1996; Cardona, Hartenstein, and Romero 2005; Bolanos and Litvaitis 2009; Rawlinson 2010; Semmler and Wanninger 2010; Krupenko and Dobrovolskij 2015). This organization originates during early embryogenesis, from an irregular network of cells projecting myofilaments in random orientation, until the first transverse circular muscles are formed (Reiter et al. 1996; Cardona, Hartenstein, and Romero 2005; Bolanos and Litvaitis 2009; Rawlinson 2010; Semmler and Wanninger 2010). The position of the first circular muscles varies between species. In some cases, a primary fiber is present (e.g., Rawlinson 2010), but in general, they do not form progressively from the anterior to the posterior end (Figure 9.3K). During ontogeny, circular muscles can be added via two different cellular processes—by duplication of the whole muscle resulting in double stranded fibers or by the branching off of one end of the fiber (Bolanos and Litvaitis 2009; Semmler and Wanninger 2010). The putative mechanisms in place to control the even distribution of these dynamic populations of circular muscles remain unknown, but it is hypothesized that interactions with the nervous system might play an important role (Rawlinson 2010).

Free-living flatworms also display some less common segmental traits, such as paired series of lateral gut diverticula alternating with gonads (Lang 1881). But perhaps one of the most striking examples of segmental organization in flatworms occurs in some of the parasitic forms—the tapeworms. Their adult body is notably divided into serially repeated morphological units delimited by external constrictions of the body wall (Figure 9.3L), which contain serially arranged internal structures, such as neurons, muscles, and gonads (Hyman 1951b; Mehlhorn et al. 1981).

These segments, or proglottids, are demarcated by annular infoldings of the syncytial tegument layer that form the tapeworm body wall (Figure 9.3M) (Mehlhorn et al. 1981). The folds are superficial and there are no internal membranous structures separating the proglottids (Mehlhorn et al. 1981; Koziol 2017). Unlike the typical segmented animals, the tapeworm segments form at a germinative zone behind the “head” (Rozario and Newmark 2015), so that the oldest proglottids are located toward the posterior end of the animal (Hyman 1951b; Mehlhorn et al. 1981). This growth zone likely undergoes a periodic accumulation of proliferative cells during segmentation (Koziol et al. 2010). Pioneering work on a tapeworm provided initial evidence that the annular infoldings of the tegument are under tight genetic control (Holy et al. 1991). The processes that establish the proglottid boundaries and how they compare to the segmentation mechanisms in other animals remain elusive, but are currently under active investigation (Koziol et al. 2016; Koziol 2017; Olson et al. 2018).

In addition to the body wall segmentation, tapeworms also display internal segmental traits that in most cases are in register with external segmental features. For example, the nervous system arrangement is stereotypic with three transverse commissures per proglottid intercepting the longitudinal nerve cords (Figure 9.3N); the circular musculature is evenly spaced along the anteroposterior axis and inner transverse cortical fibers can be present at each proglottid boundary (Figure 9.30); the excretory canals of the osmoregulatory system have a ladder-like organization (Figure 9.3P); and finally, each proglottid contains a stereotypical set of reproductive organs and a single genital pore (Rozario and Newmark 2015).

In fact, some tapeworm lineages have no proglottid boundaries and only exhibit internal segmental traits. Strikingly, the phylogeny of tapeworms suggests the segmental arrangement of internal traits evolved before the external annular infoldings in the clade (Olson et al. 2001). This indicates that the segmental organization of tapeworms was established stepwise, possibly involving independent developmental mechanisms. If and how the patterning of internal traits might have influenced the evolution of the external morphology remains an open question, and more detailed data about the development of these internal structures is needed (Koziol 2017). Given that tapeworms evolved de novo a complex segmental organization (Olson et al. 2001), the group can provide interesting insights about molecular evolution, for example, how known molecular pathways might have been coopted to pattern tapeworm segmental traits, or potentially reveal novel developmental mechanisms involved in generating repeated structures.

 
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