Morphological, Behavioral, and Molecular Characterization of Avian Schistosomes (Digenea: Schistosomatidae) in the Native Snail Chilina dombeyana (Chilinidae) from Southern Chile

Abstract

Avian schistosomes are blood flukes parasitizing aquatic birds and snails, which are responsible for a zoonotic disease known as cercarial dermatitis, a hypersensitive reaction associated to the cutaneous penetration of furcocercariae. Despite its worldwide distribution, its knowledge is fragmentary in the Neotropics, with most of data coming from Argentina and Brazil. In Chile, there are only two mentions of these parasites from birds, and one human outbreak was associated to the genus “Trichobilharzia”. However, the identity of such parasites is pending. The aim of this study was to identify the furcocercariae of avian schistosomes from Southern Chile using an integrative approach. Thus, a total of 2283 freshwater snails from different families were collected from three different regions. All snails were stimulated for the shedding of furcocercariae, but only Chilina dombeyana (Chilinidae) from the Biobío region was found to be parasitized. The morphology and phylogenetic analyses of 28S and COI genes stated two lineages, different from Trichobilharzia, shared with Argentina. This study provides new information on Neotropical schistosomes, highlighting the need for major research on these neglected trematodes, which are considered to be emerging/re-emerging parasites in other parts of the globe as consequence of anthropogenic disturbances and climatic change. Highlights: 1. Two different lineages (Lineage I and II) were described and molecularly characterized (28S and COI genes); 2. Cercaria chilinae I y II are proposed as a synonymous of Lineage II. Thus, a total of four different lineages of avian schistosomes are related to Chilina spp.; 3. Chilina spp. represents an important intermediate host for avian schistosomes in South America, constituting a reservoir de schistosomes with zoonotic potential; 4. Coinfection between the two different lineages was found, a finding previously not reported for avian schistosomes; 5. Expansion in the geographic distribution of Nasusbilharzia melancorhypha from its original record in Argentina, with Chilina dombeyana as an additional intermediate host.

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

“…Large ribosomal subunit (28S) phylogenies [ 21 , 39 , 41 ] place Macrobilharzia at the base of the SB + DAS clades, thus diverging earlier than the majority of avian schistosomatid species. Mitochondrial cox 1 studies, however, provide less consistent results [ 39 , 40 ], possibly due to the saturation of third codon positions [ 80 , 81 ]. Overall, there is a lack of sufficient detail about intermediate and definitive host use patterns and the cercarial anatomy for Macrobilharzia .…”

“…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.…”

“…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.…”

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

“…It exemplifies a schistosome inherently limited in its geographic distribution by its snail host preference, and is the only known member of the most recently erected genus Nasusbilharzia [ 22 ]. Chilina is an important host genus for avian schistosomes in South America, and co-infections of two species have even been identified from single specimens of C. dombeyana [ 82 ].…”