Biodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa)

Abstract

BackgroundMyxozoa are extremely diverse microscopic parasites belonging to the Cnidaria. Their life-cycles alternate between vertebrate and invertebrate hosts, predominantly in aquatic habitats. Members of the phylogenetically well-defined Sphaerospora (sensu stricto) clade predominantly infect the urinary system of marine and freshwater fishes and amphibians. Sphaerosporids are extraordinary due to their extremely long and unique insertions in the variable regions of their 18S and 28S rDNA genes and due to the formation of motile proliferative stages in the hosts' blood. To date, DNA sequences of only 19 species have been obtained and information on the patterns responsible for their phylogenetic clustering is limited.MethodsWe screened 549 fish kidney samples from fish of various geographical locations, mainly in central Europe, to investigate sphaerosporid biodiversity microscopically and by 18S rDNA sequences. We performed multiple phylogenetic analyses to explore phylogenetic relationships and evolutionary trends within the Sphaerospora (s.s.) clade, by matching host and habitat features to the resultant 18S rDNA trees. The apparent co-clustering of species from related fish hosts inspired us to further investigate host-parasite co-diversification, using tree-based (CoRE-PA) and distance-based (ParaFit) methods.ResultsOur study considerably increased the number of 18S rDNA sequence data for Sphaerospora (s.s.) by sequencing 17 new taxa. Eight new species are described and one species (Sphaerospora diminuta Li & Desser, 1985) is redescribed, accompanied by sufficient morphological data. Phylogenetic analyses showed that sphaerosporids cluster according to their vertebrate host order and habitat, but not according to geography. Cophylogenetic analyses revealed a significant congruence between the phylogenetic trees of sphaerosporids and of their vertebrate hosts and identified Cypriniformes as a host group of multiple parasite lineages and with high parasite diversity.ConclusionsThis study significantly contributed to our knowledge of the biodiversity and evolutionary history of the members of the Sphaerospora (s.s.) clade. The presence of two separate phylogenetic lineages likely indicates independent historical host entries, and the remarkable overlap of the larger clade with vertebrate phylogeny suggests important coevolutionary adaptations. Hyperdiversification of sphaerosporids in cypriniform hosts, which have undergone considerable radiations themselves, points to host-driven diversification.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2863-z) contains supplementary material, which is available to authorized users.

Mechanisms and Drivers for the Establishment of Life Cycle Complexity in Myxozoan Parasites

“…Here, myxozoans belonging to the Sphaerospora sensu stricto clade were sequenced for the first time from elasmobranchs. This clade is normally consistently positioned basal to oligochaete-and polychaete-infecting lineages [3,38,39] while it was reconciliated as sister to the polychaete-infecting clade, with 82% bootstrap support in both, maximum likelihood and maximum parsimony analyses, in the present study. Bipteria vetusta from Chimaera monstrosa represents the most basal lineage in polychaete-infecting myxozoans, similar to Chloromyxum spp.…”

“…This raises the question if other, evolutionarily even more ancient fish (Agnatha: cyclostomes or the extinct conodonts and ostracoderms) served as initial vertebrate hosts for the first subclade within sphaerosporids. Since this first subclade harbors exclusively marine species [38], hagfish could be a feasible ancestral host group. A single record of a myxozoan in hagfish exists [16], however DNA sequence data is missing.…”

“…A single record of a myxozoan in hagfish exists [16], however DNA sequence data is missing. On the other hand, it may well be that this first subclade distinguishes itself from the remainder of sphaerosporids due to an independent historic event of invertebrate host acquisition in an annelid stem group, such as Haplodrilii (basal polychaetes) or Sipuncula (known hosts of myxozoans without DNA sequence records [44]), much earlier in the evolution of sphaerosporids [38], when they first invaded invertebrates. Future investigations into these potential host groups likely bear exciting outcomes.…”

“…The life history of members of the fourth clade, Sphaerospora sensu stricto, is yet to be confirmed, as a single experimental study exists that identified an oligochaete as a sphaerosporid invertebrate host [48]. The reconciliation of Sphaerospora sensu stricto as a sister clade to the polychaete-infecting myxozoans is uncommon but has occasionally occurred previously [49,50] and may suggest that sphaerosporids, like members of polychaete-and oligochaete-infecting clades, emerged as parasites of annelid stem groups [3,38], rather than representing an isolated group parasitizing a different invertebrate group, such as the Malacosporeans. Malacosporeans invade freshwater bryozoans belonging to the Phylactolaemata, and though known to parasitize cyprinid and salmonid fishes, have never been found in Chondrichthyes.…”

Malacosporean myxozoans exploit a diversity of fish hosts

“…Both host species have previously been reported with sphaerosporid infections in Europe (El-Matbouli and Hoffman, 1996;Patra et al, 2018). Rounded sporogonic stages ( Fig.…”