Abstract
It is assumed that complex life cycles in cnidarian parasites belonging to the Myxozoa result from incorporation of vertebrates into simple life cycles exploiting aquatic invertebrates. However, nothing is known about the driving forces and implementation of this event, though it fostered massive diversification. We performed a comprehensive search for myxozoans in evolutionary ancient fishes (Chondrichthyes), and more than doubled existing 18S rDNA sequence data, discovering seven independent phylogenetic lineages. We performed cophylogenetic and character mapping methods in the largest monophyletic dataset and demonstrate that host and parasite phylogenies are strongly correlated, and that tectonic changes may explain phylogeographic clustering in recent skates and softnose skates, in the Atlantic. The most basal lineages of myxozoans inhabit the bile of chondrichthyans, an immunologically privileged site and protective niche, easily accessible from the gut via the bile duct. We hypothesize that feed-integration is a likely mechanism of host acquisition, an idea supported by feeding habits of chimaeras and ancient sharks and by multiple entries of different parasite lineages from invertebrates into the new host group. We provide exciting first insights into the early evolutionary history of ancient metazoan parasites in a host group that embodies more evolutionary distinctiveness than most other vertebrates.
Highlights
Parasite life cycle changes generally have adaptive components and are not purely accidental [1].Changes in life cycle complexity, i.e., the acquisition of a new host group can either be a necessary response to changes in external environmental conditions or the outcome of the differential success of alternative transmission strategies under stable external conditions, and is usually associated with evolutionary advantages [2].Biology 2020, 9, 10; doi:10.3390/biology9010010 www.mdpi.com/journal/biologyMyxozoans are a group of cnidarians that are estimated to have emerged approximately601–700 million years ago, and there is compelling evidence from phylogeny and life history, that they first settled as parasites of aquatic invertebrate hosts [3]
Kidneys and gall bladders/liver were commonly found infected with myxozoans, some muscle samples harbored parasites, no other organs tested positive by microscopy or PCR-based DNA analyses
In order to reconstruct the evolution of life cycle complexity in the Myxozoa and study the patterns of diversification in the newly acquired vertebrate host, we more than doubled existing 18S rDNA
Summary
Parasite life cycle changes generally have adaptive components and are not purely accidental [1].Changes in life cycle complexity, i.e., the acquisition of a new host group can either be a necessary response to changes in external environmental conditions or the outcome of the differential success of alternative transmission strategies under stable external conditions, and is usually associated with evolutionary advantages [2].Biology 2020, 9, 10; doi:10.3390/biology9010010 www.mdpi.com/journal/biologyMyxozoans are a group of cnidarians that are estimated to have emerged approximately601–700 million years ago (mya), and there is compelling evidence from phylogeny and life history, that they first settled as parasites of aquatic invertebrate hosts [3]. Following the occurrence of aquatic vertebrates on Earth, myxozoans implemented fish, which emerged 410–447 mya [4,5], as secondary hosts in their life cycles. This event fostered massive host-associated biodiversification [3] and likely presents the main reason for the distinct success of the Myxozoa, when compared with other parasitic cnidarians. It appears that fish were acquired as secondary hosts multiple times during myxozoan evolution [3,14]
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