The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by high species diversity. This inspired us to examine the history of adaptive radiations in myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes, and the Myxozoa, and proposed fish as original hosts for both sister lineages. We demonstrate that the Myxozoa emerged long before fish populated Earth and that phylogenetic congruence with their invertebrate hosts is evident down to the most basal branches of the tree, indicating bryozoans and annelids as original hosts and challenging previous evolutionary hypotheses. We provide evidence that, following invertebrate invasion, fish hosts were acquired multiple times, leading to parallel cospeciation patterns in all major phylogenetic lineages. We identify the acquisition of vertebrate hosts that facilitate alternative transmission and dispersion strategies as reason for the distinct success of the Myxozoa, and identify massive host specification-linked parasite diversification events. The results of this study transform our understanding of the origins and evolution of parasitism in the most basal metazoan parasites known.

Biology Centre of the Czech Academy of Sciences Institute of Parasitology České Budějovice Czech Republic

Cavanilles Institute of Biodiversity and Evolutionary Biology University of Valencia Valencia Spain

Marine Biology Department The Leon H Charney School of Marine Sciences University of Haifa Haifa Israel

References provided by Crossref.org

Comparative transcriptomics reveal stage-dependent parasitic adaptations in the myxozoan Sphaerospora molnari

Immunological memory in a teleost fish: common carp IgM+ B cells differentiate into memory and plasma cells

Solving the Myxidium rhodei (Myxozoa) puzzle: insights into its phylogeny and host specificity in Cypriniformes

Diversity of myxozoans (Cnidaria) infecting Neotropical fishes in southern Mexico

Red blood cells in proliferative kidney disease-rainbow trout (Oncorhynchus mykiss) infected by Tetracapsuloides bryosalmonae harbor IgM+ red blood cells

The Phylogenetic Position of the Enigmatic, Polypodium hydriforme (Cnidaria, Polypodiozoa): Insights from Mitochondrial Genomes

To React or Not to React: The Dilemma of Fish Immune Systems Facing Myxozoan Infections

Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Proteases as Therapeutic Targets Against the Parasitic Cnidarian Ceratonova shasta: Characterization of Molecules Key to Parasite Virulence In Salmonid Hosts

Genetic Diversity of Serine Protease Inhibitors in Myxozoan (Cnidaria, Myxozoa) Fish Parasites

Transcriptome-Wide Comparisons and Virulence Gene Polymorphisms of Host-Associated Genotypes of the Cnidarian Parasite Ceratonova shasta in Salmonids

Transcriptome of Sphaerospora molnari (Cnidaria, Myxosporea) blood stages provides proteolytic arsenal as potential therapeutic targets against sphaerosporosis in common carp

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

Selection of suitable reference genes for gene expression studies in myxosporean (Myxozoa, Cnidaria) parasites

The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari

Ortholinea concentrica n. sp. (Cnidaria: Myxozoa) from the Patagonian seabass Acanthistius patachonicus (Jenyns, 1840) (Perciformes: Serranidae) off Patagonia, Argentina

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

Life in a rock pool: Radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces

See more in PubMed

Dryad
10.5061/dryad.8f4b9