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

Astrid S Holzer,Ivan Fiala,Pavla Bartošová-Sojková,Martina Lisnerová,Cecile C Reed,Alena Lövy,Tereza Tomková,Tzen-Yuh Chiang

doi:10.1371/journal.pone.0194042

Abstract

IntroductionIntertidal rock pools where fish and invertebrates are in constant close contact due to limited space and water level fluctuations represent ideal conditions to promote life cycles in parasites using these two alternate hosts and to study speciation processes that could contribute to understanding the roles of parasitic species in such ecosystems.Material and methodsGall bladder and liver samples from five clinid fish species (Blenniiformes: Clinidae) were morphologically and molecularly examined to determine the diversity, prevalence, distribution and host specificity of Ceratomyxa parasites (Cnidaria: Myxozoa) in intertidal habitats along the coast of South Africa. Phylogenetic relationships of clinid ceratomyxids based on the SSU rDNA, LSU rDNA and ITS regions were assessed additionally to the investigation of population genetic structure of Ceratomyxa cottoidii and subsequent comparison with the data known from type fish host Clinus cottoides.Results and discussionSeven Ceratomyxa species including previously described Ceratomyxa dehoopi and C. cottoidii were recognized in clinids. They represent a diverse group of rapidly evolving, closely related species with a remarkably high prevalence in their hosts, little host specificity and frequent concurrent infections, most probably as a result of parasite radiation after multiple speciation events triggered by limited host dispersal within restricted spaces. C. cottoidii represents the most common clinid parasite with a population structure characterized by young expanding populations in the south west and south east coast and by older populations in equilibrium on the west coast of its distribution. Parasite and fish host population structures show overlapping patterns and are very likely affected by similar oceanographic barriers possibly due to reduced host dispersal enhancing parasite community differentiation. While fish host specificity had little impact on parasite population structure, the habitat preference of the alternate invertebrate host as well as tidal water exchange may be additional crucial variables affecting the dispersal and associated population structure of C. cottoidii.

Highlights

Intertidal rock pools where fish and invertebrates are in constant close contact due to limited space and water level fluctuations represent ideal conditions to promote life cycles in parasites using these two alternate hosts and to study speciation processes that could contribute to understanding the roles of parasitic species in such ecosystems
Myxospores (Fig 2A–2E) and/or plasmodia (Fig 2F) of the genus Ceratomyxa were found in 40% of examined samples with the majority represented by infected gall bladders (58/152), and with few of them (3/152) found in bile ducts
Phylogenetic positioning of clinid ceratomyxids within the Ceratomyxa clade The Ceratomyxa clade is an assemblage of diverse groups that evolved initially at different substitution rates and some of them have undergone subsequent radiation events [46]. This pattern is evident in ceratomyxids from South African clinids that clustered into a single wellsupported long-branched lineage (“Ceratomyxa group from clinid fish“) which further split into several short-branched species (Fig 3)

Summary

Objectives

Our aims were to i) examine diversity, prevalence, distribution and host species spectra of ceratomyxids from South African clinids, ii) reconstruct the phylogenetic relationships among clinid ceratomyxids and to other members of the Ceratomyxa clade, and iii) reveal the patterns of population structuring of C. cottoidii and to investigate if they are linked to geographical or host-driven isolation of parasite populations

Methods

Results

Discussion

Conclusion