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 exceptionally high species diversity. This inspired us to examine the history of reciprocal interactions and 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 clearly 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 hypothesis. 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.

Trees for cophylogeny reconciliationHost and parasite trees (24) used for cophylogeny reconciliation and based on the alignments of 18S rDNA and 16S rRNA gene sequences deposited in the same dryad folder.trees for cophylogeny reconciliation.nexMolClock_alignmentAlignment of 6 concatenated protein-coding genes, i.e. aldolase (200 aa), triosephosphate isomerase (217 aa), phosphofructokinase (175 aa), methionine adenosyltransferase (348 aa), elongation factor 1 alpha (418 aa) and ATP synthase beta chain (430 aa), for molecular clock analysis of myxozoan and other metazoan taxa.18S rDNA aligment_myxozoans_in_vertebrate_hostsCut alignment of 18S rDNA sequences of 682 taxa of myxozoans from vertebrate hosts in fasta format18S_myxozoans_in_vertebrate_hosts.fasta18S rDNA_myxozoans_from_invertebrate_hostsCut alignment of 18S rDNA sequences of 124 taxa of myxozoans from invertebrate hosts in fasta format18S_myxozoans_from_invertebrates_53M.fasta18S rDNA alignment_invertebrate hostsCut alignment of 18S rDNA sequences of 25 taxa of invertebrate hosts of myxozoans in fasta format18S_invertebrate hosts.fasta16S rRNA_vertebrate_hostsCut alignment of 16S rRNA gene sequences of 246 taxa of vertebrate hosts of myxozoans in fasta format16S_vertebrate_hosts.fastafull__mitogenome_vertebrate_hostsCut alignment of full mitogenome sequences of 105 taxa of invertebrate host families of myxozoans in fasta format