Reproduction and Development in Platyhelminthes

T. J. Pandian

• Publisher: CRC Press
• Year: 2020
• ISBN:
  9781000054903
• Edition: 1
• Topic: Physical Sciences
• Subtopic: Oceanography

This book is a comprehensive elucidation on aspects of reproduction and development in platyhelminthes covering from acoelids to taeniids. With the unique presence of neoblasts, turbellarians serve as a model for studies on cancer and senescence. Of ~ 27, 000 species, ~ 77% are parasites; they are harmful to man and his food basket from livestock and fish. The stress hormone, cortisol level is responsible for susceptibility and resistance of the host. In digeneans, the propagatory multiplication potency is retained by all the larval forms and in either direction in sporocyst. The higher clonal diversity, mixing and selection in Second Intermediate Host (SIH) may purge inbreeding depression suffered by the fluke on propagatory multiplication in First Intermediate Host (FIH). Of 12, 012 digeneans, 88% may engage 33, 014 potential SIH species. They have the choice to select one among the available/awaiting 3.5 host species. The motility of vertebrate host and euryxenic flexibility/scope for selection of SIH species has increased lineage diversification in digeneans. The life cycle of cestodes is divided into aquatic and terrestrial patterns. The former includes (i) oncosphere and (ii) coracidium types and the latter (iii) hexacanth-cysticercoid, (iv) hexacanth-tetrathyridium and (v) hexacanth-cysticercus types. The share for the oncosphere, coracidium and hexacanth types is 17.0, 29.5 and 46.5%, respectively. The staggering fecundity and adoption of the intermediate host in the herbivorous/insectivorous food chain have enriched Taenioidea as the most (2, 264) speciose order. Sex specific genes Smed-dmd 1 and macbol have been identified, and neuropeptides and dipeptides are involved in sexualization. Trematodes are unable to parasitize elasmobranchs, as they cannot suck body fluid/blood containing a high level of urea. Relatively higher fecundity supplemented with propagatory multiplication, incorporation of SIH in 88% species, clonal selection in SIH, and euryxenic flexibility and the widest choice for selection of SIH have led to the highest lineage diversification to render digeneans as the most speciose order in Platyhelminthes.

1

General Introduction

Introduction

THE phylum Platyhelminthes comprises free-living flatworms (turbellarians), and parasitic flukes (ectoparasitic monogeneans and endoparasitic digeneans) and tapeworms (endoparasitic cestodes). The platyhelminths are bilaterally symmetrical, dorso-ventrally flattened, triploplastic, acoelomic, mostly hermaphroditic, soft-bodied worms with either branched ‘blind gut’ tasked with digestion and distribution of nutrients or no gut (Fig. 1.1). They lack respiratory and circulatory systems and instead rely on diffusion to obtain oxygen. The following hallmark traits elevate them as unique in animal kingdom: (i) hermaphroditism, (ii) ectolecithal egg production, by separation of the ovary and vitellogenic glands and (iii) renewal of all somatic cell types, which cannot undergo mitosis, once their differentiation is completed (see Section 2.8). Consequently, the flatworms exist in a dynamic steady state between the single proliferating cell type and multiple shortlived differentiated cell types (Rink, 2013).

Thanks to the presence of pluripotent neoblasts, the turbellarian planarians are known for the extraordinary potency for regeneration and clonal reproduction. The planarian neoblasts serve as a model system to understand the proliferative control of stem cell, which is relevant to human cancers. Firstly, studies on planarian ortholog of the human tumor suppressor PTEN have revealed that RNAi-mediated knockdown leads to neoblast hyper-proliferation of the TOR signaling pathway. These disease-relevant genetic pathways in planarians may provide many keys to the homeostatic control of cell proliferation. Secondly, senescence in animals has been traced to the progressive shortening of telomeres following each round of DNA replication. Neoblasts seem to have overcome the end of replication problem indefinitely to facilitate their immortality. Hence, planarians may serve as a potential model system to understand how the diseased, damaged and ageing tissues can be regenerated (see Aboobaker, 2011).

FIGURE 1.1
A. Ectocommensalic acoelid Ectocotyle paguri (after E.G. Richard), B. rhabdocoel Microstomum, C. Dugesia tigrina (from Hyman, 1951), D. Temnocephala (after Haswell, 1893), E. Land planarian Bipalium kewense and F. Polystomoides (after Stunkard, 1917). G. Rajonchocotyle (after Muller and Van Cleave, 1932), H. Opisthorchis sinensis (after A.E. Galigher), I. Diplostomum (after Dubois, 1938), J. Schistosoma haematobium (after Looss, 1990). K. Lithobium aenigmaticum (from Caira et al., 2014), L. Taenia (after Olsen, 1939), M. Echinococcus granulosus (after Southwell, 1930), N. Gyrocotyle and O. T. saginata (from Hyman, 1951) (All figures are free hand drawings).

Many vertebrate species serve as definitive or final host for the approximately 21,330 speciose flukes and tapeworms. The digenean flukes and cestodes engage a large number of intermediate host species. In these parasites, sexual reproduction occurs in vertebrate hosts but parthenogenic (or polyembryonic, see Galaktinov and Dobrovolskij, 2003, Littlewood et al., 2015, clonal, see p 158) multiplication occurs in invertebrate hosts, of which most of them are molluscs, and rarely annelids. For example, a single miracidium, the first larva to emerge from a fertilized egg of the digenean flukes after passing through propagatory multiplication in sporocyst and/or redia, is capable of producing more than a million cercariae (e.g. strigeids, see Hyman, 1951), the final or penultimate larva to infect the vertebrate host. The number of eggs and protoscoleces produced by a hydatid cyst of Echinococcus granulosus measuring 5 ml is an astonishing 25 million/day (Smyth, 1964).

The following examples may reveal the magnitudes of health problems emanating from these platyhelminth parasites: (i) Schistosomiasis, caused by the blood fluke Schistosoma spp, is the second most common disease in the world and is widespread in 70 subtropical countries. More than 200 million people are infected by the disease and an estimated 779 millions are at the risk of infection and ~ 200,000 die annually (see Pandian, 2017). Whereas not more than 0.7% die following malarial infection, ~ 10% of schistosome-infected patients succumb to death. Hence, the global expenditure on schistosomiasis amounts to US$ 67 million. Between 1980 and 2014 alone, 14,933 research articles were published on these parasites (Jurberg and Brindley, 2015). Available information shows the enormous cost and/or loss incurred by some countries and the world at large due to the platyhelminthic diseases to humans and their food basket from livestock and fish (Table 1.1). The loss suffered by livestock is assessed from the reduced yield of milk and meat, growth and fertility as well as increased morbidity and mortality. Global economic losses due to fasciolosis are estimated at ~ US$ 2.5 billion annually. A more recent study has estimated the loss of US$ 4.9 billion for India alone (see McCusker et al., 2016). Notably, the implementation of hygienic practices ranges from condemnation of fasciolosis-infected liver in a small developing African Ethiopia to others, where the meat/beef is not inspected and certified prior to marketing. For example, no information is available on implementation of hygienic practices on marketed meat in large developing Asian country like India. Sangunicoliasis is an important disease caused by Sanguinicola inermis in aquaculture farms. Unfortunately, the debilitated fish cannot be treated (see Pandian, 2017). An estimate suggests the possible presence of 25,000 monogenean parasitic species, i.e. the monogeneans are as speciose as teleostean fish are (Whittington, 1998). Despite the great aquaculture potency of China and India, Brazil seems to be the only country, which has made estimates on the loss due to ectoparasitic crustaceans and monogeneans in aquaculture farms. Briefly, the volume of loss due to health problems posed to human, livestock and fish is so huge and fluctuates widely between countries. Food and Agriculture Organization (FAO) has not been able to make a global estimate, as many countries either do not implement hygienic practices to check the health status of meat/beef or do not have valid data on the loss. Notably, aquaculture is perceived to have the greatest potential to produce more and good quality aquatic food (FAO, 2014). In aquaculture farms, efforts are made to produce more and more fish with less and less water. A consequence of this can increase the scope for infection by monogenean parasites. The foregone account may impress on the relevance of turbellarian stem cells for studies on cancer and senescence as well as that of parasitic trematodes and cestodes on the cost of human health and loss to his food basket from livestock and fish. Among invertebrates, Platyhelminthes ranks first, as they are harmful to man and cause heavy loss to his food basket.

Not surprisingly, many books on platyhelminths have been authored or edited. However, most of them are limited to one or other taxonomic group(s) or to a specific theme. For example, half a dozen books are available on regeneration and clonal reproduction in turbellarians (e.g. Brondsted, 1969); a few are also available on the biology and evolution of the flukes (e.g. Galaktinov and Dobrovolskij, 2003) and diseases and management of tapeworms (e.g. Muller, 2001). This book is a comprehensive synthesis of relevant aspects of reproduction and development in platyhelminths covered from Acoela to Taenioidea. With availability of voluminous literature, it provides a ‘snap-shot’ of biological aspects of platyhelminths rather than an in depth or exhaustive account on diagnostics and management of platyhelminth diseases.

TABLE 1.1
Representative examples for the incidence and estimated cost or loss caused by parasitic platyhelminths. mil = million, bil = billion, y = year

Disease	Host	Country	Reported observations	Reference
Incidence
Schistosomiasis	Human		200 mil infected, 0.2 mil die	see Pandian (2017)
Fasciolosis	Cattle	Global	1.7 mil bovines infected
	Human	Global	35 mil people infected, especially in the Chinese countries	Lim (2011)
	Cattle	India	30–80% incidence	Gupta and Singh (2002)
Helminths	Human Poultry	Global Egypt	40 mil infected 14% (geese), 38% (ducks), 42% (turkeys), 46% (fowls) and 52% pigeons are infected	A. Payne (Facebook) Nagwa et al. (2013)
Cost and Loss
Fasciolosis	Human	USA	Costs 100 mil US$/y	Roberts et al. (1994)
	Sheep	Ethiopia	Loss amounts to 114,678 $/y	Ayalneh et al. (2018)
	Sheep & Goats	Global Australia	Loss is 2.5 bil €/y Loss is 50–80 mil €/y	Love (2017) Boray (2007)
	Cattle	Ethiopia	Infected liver condemnation costs 8312 $/y	Abebe et al. (2010)
	Cattle	Switzerland	Loss @ 299 €/infected cattle/y costs 50 mil €/y	Dorchies (2007), Schweizer et al. (2005)
	Cattle	England	Loss is 23 mil £/y	Mazeri et al. (2016)
	Cattle	USA	Loss is 5 mil US$/y	Malone (1986)
	Cattle	Uttarkhand, India	900 mil Rs/y on milk yield alone in a small state	Bardhan et al. (2014)
	Cattle	India	Estimated loss is 4.86 bil/y	McCusker et al. (2016)
Taeniasis Cysticercosis	Human Human	USA USA	Cost 0.3 mil $/y with lowest (0.06%) Incidence. cf 12% incidence in Laos 7% incidence costing 0.8 mil $/y	Roberts et al. (1994) Roberts et al. (1994)
Parasites	Fishes	Global Brazil	Loss is 84 mil $/y Loss is 5 mil $/y	Tavares-Dias and Martins (2017), Shinn et al. (2015)

1.1 Taxonomy and Diversity

According to Hyman (1951), the phylum Platyhelminthes is classified into three classes namely Turbellaria, Trematoda and Cestoda; the trematodes are divided into two major orders: Monogenea and Digenea (Table 1.2). Further divisions of them have been subjected to many changes, which are described in the respective chapters.

Phylogeny traces the origin and evolution of taxonomic groups. Of theories proposing the origin of polyclad from ctenophores and acoeloid from planuloids, the second one is more a...