Schistosomes from the Persian Gulf: phylogenetic relationships, host associations and life-cycle elucidation of Ornithobilharzia canaliculata (Rudolphi, 1819) Odhner, 1912

Abstract

Background: Avian schistosomes comprise a diverse and widespread group of trematodes known for their surprising ability to switch into new hosts and habitats. Their cercariae are the causative agents of the waterborne allergic disease cercarial dermatitis. There are 13 recognised genera of avian schistosomes with majority of the extant species with freshwater-based life-cycles. Despite the considerable research attention on avian schistosomes much less it is known about the diversity, geographical range and host associations of the marine representatives. Here, we provide novel data on the species diversity and host-parasite relationships of the marine schistosomes in respect to their intermediate gastropod host from the Persian Gulf. Methods: A total of 1,745 horn snails of Pirenella cingulata (Gmelin), were examined during a survey from December 2019 to February 2020 from eight distinct locations along the coast of Iran. Partial sequences of the mitochondrial cytochrome c oxidase subunit 1 (cox1) and the nuclear 28S rRNA gene were generated for the schistosome isolates recovered and used for molecular identification and phylogenetic reconstruction. Results: Our molecular analyses inferred from both molecular markers revealed presence of two schistosome species, Ornithobilharzia canaliculata (Rudolphi, 1819) Odhner, 1912 and a putative new species of Austrobilharzia Johnston, 1917. Molecular elucidation of the life-cycle of O. canaliculata was achieved for the first time via matching novel and published sequence data from adult and larval stages. This is the first record of Ornithobilharzia from the Persian Gulf and globally the first record of this genus in a potamidid snail host.Conclusions: The present study provides new host and distribution records for major etiological agents of cercarial dermatitis and contributes important information on host-parasite relationships. Our study further highlights the importance of the molecular systematics in the assessment of schistosome diversity and calls for further surveys in order to reach a better understanding of the schistosome diversity and patterns of relationships among them, host associations, transmission strategies and distribution coverage.

Scratching the Itch: Updated Perspectives on the Schistosomes Responsible for Swimmer’s Itch around the World

“…For instance, the species indicated, T. physellae , is indigenous to North America but has recently been reported in Europe, exploiting the introduced physid snail that has established there [ 77 ]. Khosravi et al [ 78 ] report a similar cosmopolitan distribution for the marine schistosome Ornithobilharzia canaliculata .…”

“…This version would be favored if the essential snail host species (such as Physa ) were ubiquitously common, and adult schistosomes were long-lived or new worms successfully colonized already-infected hosts. This would seem to create the opportunity for panmictic schistosome populations, and some evidence, as for the cosmopolitan T. querquedulae with little population structure [ 76 ], supports this notion, as do studies of avian schistosomes using marine gastropods [ 29 , 78 ]. Another possibility is that the input of schistosome eggs of migrating subadults or adults is not as pronounced, and that snail infections originate mostly from resident birds and their progeny, placing considerable emphasis on the vulnerability of young birds to infection.…”

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

“…A fourth subfamily, Griphobilharziinae Platt, Blair, Purdie & Melville, 1991, containing a single species Griphobilharzia amoena , has been recognized, but sequence-based data places this species within the Spirorchiidae [ 36 ]. Molecular phylogenies have not supported these subfamily designations [ 21 , 25 , 26 , 27 , 31 , 34 , 37 , 38 , 39 ], and the most appropriate subfamily classifications remain unclear.…”

“…As illustrated by the conflicting results from prior studies ( Table 1 ), the continued sequencing of 500–1500 bp markers seems unlikely to resolve deeper schistosomatid relationships. New methodologies are needed to resolve the following pivotal nodes and groups, and thus better characterize diversification, evolution of host-use, host switches and divergence times within Schistosomatidae: AO Clade: Marine avian genera, Austrobilharzia and Ornithobilharzia (AO clade), are often recovered as well-supported sister genera [ 36 , 39 , 40 ], and both are considered globally distributed. In most of the studies over the last 10 years, the AO clade typically acts as a sister group to the remainder of the schistosomatids.…”

“… DAS Clade: The derived avian–schistosomatid (DAS) clade includes the majority of avian-infecting genera ( Anserobilharzia , Allobilharzia , Bilharziella , Dendritobilharzia , Gigantobilharzia , Marinabilharzia , Nasusbilharzia , Riverabilharzia , Trichobilharzia ) and several yet-to-be described genera. The monophyly of DAS is consistently supported ( Table 1 , [ 39 , 40 ]), though its placement as a sister to the SB clade or North American mammalian schistosomatids is unclear. The relationships within the DAS clade are largely unresolved.…”