110
early diverging metazoans and sister to Bilateria, with the Ctenophora and Porifera
variously placed as earlier diverging sister lineages to Metazoa (e.g. Ryan et al.
2013; Simion et al. 2017; Whelan et al. 2017). Accordingly, cnidarians have a convincing fossil record dating from the early Cambrian (e.g. Dong et al. 2013) and, as
discussed later, with probable representation even earlier in the Ediacaran Period.
Although mainly viewed as marine animals, a few cnidarians have invaded freshwater habitats (Jankowski et al. 2008), including the model organism Hydra. In
addition, parasitic lifestyles have been adopted on several occasions by different
cnidarian lineages. One parasitic group in particular—the Myxozoa—has undergone extensive radiation as endoparasites with complex life cycles, exploiting invertebrate and vertebrate hosts. According to the most recent estimate, myxozoans
represent some 20% (2596/14,355) of all described cnidarian species (Okamura
et al. 2018), a proportion expected to rise further in view of extensive
undersampling.
This chapter reviews the evolution, origins and diversification of parasitic cnidarians. We first describe the variety of cnidarian parasites known to date and highlight
cnidarian features that may be generally conducive for adopting parasitic lifestyles.
We then focus on the major clade of parasitic cnidarians, the Endocnidozoa, which
contains the diverse Myxozoa and the monotypic Polypodium hydriforme. This
leads us to consider more explicitly pathways to endoparasitism, origins and early
hosts, and patterns and drivers of diversification within the Endocnidozoa.
4.2 Parasitic Cnidarians Other than Endocnidozoans
According to current views of cnidarian systematics (Fig. 4.2; Kayal et al. 2018)
parasitic forms have evolved at least twice in Anthozoa (Rodríguez et al. 2014) and
perhaps twice or more in Hydrozoa (Bentlage et al. 2018; Table 4.1). In all cases
parasitic stages are associated with pelagic animal hosts. They have been described
in the distantly-related burrowing anemone families, Edwardsiidae and Haloclavidae
(Rodríguez et al. 2014), and in families belonging to the hydrozoan orders
Narcomedusae and Anthoathecata (Collins et al. 2008; Bentlage et al. 2018).
Infection is likely generally to occur via the larval (planula) stage (Boero and
Bouillon 2005) with parasites then undergoing further development (Table 4.1). For
example, larvae of the anthozoan Peachia develop to polyps on their medusa hosts,
which then drop off to take up benthic existence. Polyp stages of hydrozoan narcomedusae develop as endoparasites in medusa and polychaete hosts prior to assuming life as free-living medusae. Other hydrozoans develop as ectoparasitic colonies
on fish, copepods and pteropods during the polyp phase of the life cycle. It is argued
that the anthozoan Edwardsiella lineata develops in the digestive cavity of ctenophores as a novel life history stage. The latter is inferred on the basis of a unique
combination of features (no cilia or tentacles but possessing a pharynx, retractor
muscles and mesenteries), tissue remodelling (including apoptosis), and a clear shift
B. Okamura and A. Gruhl
early diverging metazoans and sister to Bilateria, with the Ctenophora and Porifera
variously placed as earlier diverging sister lineages to Metazoa (e.g. Ryan et al.
2013; Simion et al. 2017; Whelan et al. 2017). Accordingly, cnidarians have a convincing fossil record dating from the early Cambrian (e.g. Dong et al. 2013) and, as
discussed later, with probable representation even earlier in the Ediacaran Period.
Although mainly viewed as marine animals, a few cnidarians have invaded freshwater habitats (Jankowski et al. 2008), including the model organism Hydra. In
addition, parasitic lifestyles have been adopted on several occasions by different
cnidarian lineages. One parasitic group in particular—the Myxozoa—has undergone extensive radiation as endoparasites with complex life cycles, exploiting invertebrate and vertebrate hosts. According to the most recent estimate, myxozoans
represent some 20% (2596/14,355) of all described cnidarian species (Okamura
et al. 2018), a proportion expected to rise further in view of extensive
undersampling.
This chapter reviews the evolution, origins and diversification of parasitic cnidarians. We first describe the variety of cnidarian parasites known to date and highlight
cnidarian features that may be generally conducive for adopting parasitic lifestyles.
We then focus on the major clade of parasitic cnidarians, the Endocnidozoa, which
contains the diverse Myxozoa and the monotypic Polypodium hydriforme. This
leads us to consider more explicitly pathways to endoparasitism, origins and early
hosts, and patterns and drivers of diversification within the Endocnidozoa.
4.2 Parasitic Cnidarians Other than Endocnidozoans
According to current views of cnidarian systematics (Fig. 4.2; Kayal et al. 2018)
parasitic forms have evolved at least twice in Anthozoa (Rodríguez et al. 2014) and
perhaps twice or more in Hydrozoa (Bentlage et al. 2018; Table 4.1). In all cases
parasitic stages are associated with pelagic animal hosts. They have been described
in the distantly-related burrowing anemone families, Edwardsiidae and Haloclavidae
(Rodríguez et al. 2014), and in families belonging to the hydrozoan orders
Narcomedusae and Anthoathecata (Collins et al. 2008; Bentlage et al. 2018).
Infection is likely generally to occur via the larval (planula) stage (Boero and
Bouillon 2005) with parasites then undergoing further development (Table 4.1). For
example, larvae of the anthozoan Peachia develop to polyps on their medusa hosts,
which then drop off to take up benthic existence. Polyp stages of hydrozoan narcomedusae develop as endoparasites in medusa and polychaete hosts prior to assuming life as free-living medusae. Other hydrozoans develop as ectoparasitic colonies
on fish, copepods and pteropods during the polyp phase of the life cycle. It is argued
that the anthozoan Edwardsiella lineata develops in the digestive cavity of ctenophores as a novel life history stage. The latter is inferred on the basis of a unique
combination of features (no cilia or tentacles but possessing a pharynx, retractor
muscles and mesenteries), tissue remodelling (including apoptosis), and a clear shift
B. Okamura and A. Gruhl