137
suggest that the apparently contradictory evidence for the Devonian appearance of
acipenseriform fish hosts of Polypodium (419–395 Ma) and their molecular clock
estimate of a much earlier origin for the divergence of Polypodium/Myxozoa
(651 Ma) is a result of long branch attraction. This view ignores the possibilities of
host switching or prolonged existence as free-living forms. Furthermore, none of
the specific arguments raised in support of these scenarios are convincing. These
include: large differences in genome sizes of Polypodium and the myxosporean
Kudoa iwatai; differences in gene content in myxozoans and Polypodium; comparative differences in orthologous genes of K. iwatai, Polypodium and free-living cnidarians; putative differences in stages that invade hosts (‘binucleate cells’), and;
contrasting diversities of Polypodium and myxozoans. We consider these in order as
follows:
• Genome sizes are notoriously variable and they are often reduced in parasitic
organisms (e.g. Tsai et al. 2013; Poulin and Randhawa 2015). The larger genome
size of Polypodium may thus reflect inclusion of a free-living stage in the life
cycle. Furthermore, the genome size of the myxozoan Thelohanellus kitauei is
8× larger (188.5 Mb) than that of K. iwatai (and is some 33% of the genome size
of Polypodium).
• Described differences in gene content between Polypodium and myxozoans (e.g.
reductions of genes related to development, cell differentiation and cell-cell
communication in myxozoans) can be explained by retention of a free-living
stage in Polypodium. In addition, the comparison so far only includes myxosporeans, which show a higher degree of simplification, whereas the morphologically more complex malacosporeans may have retained more of these genes.
• The highlighted lower overlap in exclusive orthologous genes (OGs) between
K. iwatai and Polypodium than between K. iwatai and two free-living cnidarians
(Nematostella vectensis and Hydra magnipapillata) is based on relatively low
numbers (24 with Polypodium, 44 with N. vectensis, 31 with H. magnipapillata).
Such variation could reflect any number of processes (e.g. patterns of gene loss,
gene assembly, contamination (e.g. see Kayal et al. 2018), etc.).
• Binucleate cells in Polypodium are described as ‘a larval, diploid stage’ that
invades fish hosts and those in myxozoans as haploid cells that invade annelid
hosts. Both the descriptions and juxtapositions are flawed. Polypodium binucleate cells that invade fish are haploid (Raikova 1994, 2008; and see earlier discussion) and myxozoan stages that invade both fish and annelid hosts are cell-in-cell
complexes (Feist et al. 2015; and see earlier discussion). Furthermore, in malacosporeans unicellular haploid stages invade bryozoan hosts.
• There are precedents for extensive radiation in one parasitic lineage and little in
its sister taxon within parasite clades. For example, the Aspidogastrea (with
some 80 species) is sister to the Digenea (with >10,000 species) (Cribb et al.
2003). Such patterns of radiations are likely explained by unique, lineage- specific
key innovations (see section 4.7.2). The argument that different patterns of diversification signify independently evolved lineages is therefore not necessarily
convincing. In addition, the monotypic status of Polypodium may partly be an
4 Evolution, Origins and Diversification of Parasitic Cnidarians
suggest that the apparently contradictory evidence for the Devonian appearance of
acipenseriform fish hosts of Polypodium (419–395 Ma) and their molecular clock
estimate of a much earlier origin for the divergence of Polypodium/Myxozoa
(651 Ma) is a result of long branch attraction. This view ignores the possibilities of
host switching or prolonged existence as free-living forms. Furthermore, none of
the specific arguments raised in support of these scenarios are convincing. These
include: large differences in genome sizes of Polypodium and the myxosporean
Kudoa iwatai; differences in gene content in myxozoans and Polypodium; comparative differences in orthologous genes of K. iwatai, Polypodium and free-living cnidarians; putative differences in stages that invade hosts (‘binucleate cells’), and;
contrasting diversities of Polypodium and myxozoans. We consider these in order as
follows:
• Genome sizes are notoriously variable and they are often reduced in parasitic
organisms (e.g. Tsai et al. 2013; Poulin and Randhawa 2015). The larger genome
size of Polypodium may thus reflect inclusion of a free-living stage in the life
cycle. Furthermore, the genome size of the myxozoan Thelohanellus kitauei is
8× larger (188.5 Mb) than that of K. iwatai (and is some 33% of the genome size
of Polypodium).
• Described differences in gene content between Polypodium and myxozoans (e.g.
reductions of genes related to development, cell differentiation and cell-cell
communication in myxozoans) can be explained by retention of a free-living
stage in Polypodium. In addition, the comparison so far only includes myxosporeans, which show a higher degree of simplification, whereas the morphologically more complex malacosporeans may have retained more of these genes.
• The highlighted lower overlap in exclusive orthologous genes (OGs) between
K. iwatai and Polypodium than between K. iwatai and two free-living cnidarians
(Nematostella vectensis and Hydra magnipapillata) is based on relatively low
numbers (24 with Polypodium, 44 with N. vectensis, 31 with H. magnipapillata).
Such variation could reflect any number of processes (e.g. patterns of gene loss,
gene assembly, contamination (e.g. see Kayal et al. 2018), etc.).
• Binucleate cells in Polypodium are described as ‘a larval, diploid stage’ that
invades fish hosts and those in myxozoans as haploid cells that invade annelid
hosts. Both the descriptions and juxtapositions are flawed. Polypodium binucleate cells that invade fish are haploid (Raikova 1994, 2008; and see earlier discussion) and myxozoan stages that invade both fish and annelid hosts are cell-in-cell
complexes (Feist et al. 2015; and see earlier discussion). Furthermore, in malacosporeans unicellular haploid stages invade bryozoan hosts.
• There are precedents for extensive radiation in one parasitic lineage and little in
its sister taxon within parasite clades. For example, the Aspidogastrea (with
some 80 species) is sister to the Digenea (with >10,000 species) (Cribb et al.
2003). Such patterns of radiations are likely explained by unique, lineage- specific
key innovations (see section 4.7.2). The argument that different patterns of diversification signify independently evolved lineages is therefore not necessarily
convincing. In addition, the monotypic status of Polypodium may partly be an
4 Evolution, Origins and Diversification of Parasitic Cnidarians