Redescription and Molecular Assessment of Relationships Among Three Species of Echeneibothrium (Rhinebothriidea: Echeneibothriidae) Parasitizing the Yellownose Skate, Dipturus chilensis, in Chile

J Parasitol. 2017 Jun;103(3):268-284. doi: 10.1645/16-177. Epub 2017 Mar 10.

Abstract

Much progress has recently been made in revising the taxonomic assignments of genera originally classified in the polyphyletic "Tetraphyllidea." Many of these genera, including Echeneibothrium, were accommodated in the order Rhinebothriidea. However, beyond this larger taxonomic action, little work has been conducted on this genus over the past 50 yr. Consequently, the criteria used for characterizing species of Echeneibothrium have lagged behind those typically used in more modern descriptions of elasmobranch-hosted cestode taxa. A series of collecting trips to Chile to obtain cestodes from the yellownose skate, Dipturus chilensis , provided a unique opportunity to apply modern morphological and molecular methods to investigate the 3 species of Echeneibothrium reported parasitizing this skate, specifically Echeneibothrium megalosoma, Echeneibothrium multiloculatum, and Echeneibothrium williamsi. In addition to redescribing all 3 species, using morphological data from light and scanning electron microscopy, maximum likelihood and bayesian inference phylogenetic analyses of the D1-D3 regions of the 28S rDNA gene were conducted to assess their relationships among other echeneibothriids for which comparable data are available. Sequencing of 59 specimens representing these 3 species of Echeneibothrium allowed us to assess the intra- and interspecific variation in the 28S rDNA gene. The redescriptions use standardized terminology for scolex morphology, proglottid anatomy, and microthrix forms and pattern; they also expand on the original descriptions to include data on scolex size, ovary size, vas deferens and vaginal configurations, testes arrangement, and genital pore position. Our morphological work led to a major reinterpretation of the scolex morphology with the recognition that all 3 species bear an apical bothridial sucker, rather than an apical loculus, prompting emendation of the diagnosis for the family Echeneibothriidae. The presence of a band of spinitriches at the apex of the apical modification of the scolex proper seems to represent an important feature for distinguishing the 2 portions of the myzorhynchus across species. Intraspecific variation ranged from 0 to 7 bp across species and interspecific variation ranged from a low of 39-46 bp between E. williamsi and E. multiloculatum to a high of 61-66 bp between E. multiloculatum and E. megalosoma. Phylogenetic analyses indicate that the 3 species of Echeneibothrium hosted by the yellownose skate are not each other's closest relatives, suggesting multiple colonization events of D. chilensis have occurred. Further phylogenetic investigation is also likely to confirm the status of the genus Pseudanthobothrium as a synonym of Echeneibothrium because its species generally group among members of Echeneibothrium.

MeSH terms

  • Animals
  • Cestoda / classification*
  • Cestoda / genetics
  • Cestoda / ultrastructure
  • Cestode Infections / epidemiology
  • Cestode Infections / parasitology
  • Cestode Infections / veterinary*
  • Chile / epidemiology
  • DNA, Helminth / chemistry
  • DNA, Helminth / isolation & purification
  • DNA, Ribosomal / chemistry
  • Fish Diseases / epidemiology
  • Fish Diseases / parasitology*
  • Intestines / parasitology
  • Likelihood Functions
  • Microscopy, Electron, Scanning / veterinary
  • Pacific Ocean / epidemiology
  • Phylogeny
  • Polymerase Chain Reaction
  • Prevalence
  • RNA, Ribosomal, 28S / genetics
  • Skates, Fish / parasitology*

Substances

  • DNA, Helminth
  • DNA, Ribosomal
  • RNA, Ribosomal, 28S