DNA Multi-Marker Genotyping and CIAS Morphometric Phenotyping of Fasciola gigantica-Sized Flukes from Ecuador, with an Analysis of the Radix Absence in the New World and the Evolutionary Lymnaeid Snail Vector Filter
by
, , , , , and
Maria Dolores Bargues
1,*
,
Maria Adela Valero
1
,
Gabriel A. Trueba
2, 
Marco Fornasini
3,
Angel F. Villavicencio
4,
Rocío Guamán
4
,
Alejandra De Elías-Escribano
1,
Ignacio Pérez-Crespo
1,
Patricio Artigas
1
and
Santiago Mas-Coma
1,*
1
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andres Estelles s/n, 46100 Valencia, Spain
2
Instituto de Microbiología, Edificio Eugenio Espejo, EE-125, Colegio de Ciencias Biológicas y Ambientales, Campus Cumbayá, Universidad San Francisco de Quito, Av. Diego de Robles y Vía Interoceánica, Quito 170901, Ecuador
3
Escuela de Medicina, Universidad Internacional del Ecuador, Av. Jorge Fernández s/n y Av. Simón Bolivar, Quito 170411, Ecuador
4
Departamento de Ciencias de la Vida y Agricultura, Universidad de las Fuerzas Armadas-ESPE, Sede Santo Domingo de los Tsáchilas, Vía Santo Domingo-Quevedo km 24, Santo Domingo de los Tsáchilas, P.O. Box 171-5-231B, Luz de América 230118, Ecuador
*
Authors to whom correspondence should be addressed.
Animals 2021, 11(9), 2495; https://doi.org/10.3390/ani11092495
Submission received: 8 July 2021
/
Revised: 13 August 2021
/
Accepted: 22 August 2021
/
Published: 25 August 2021
(This article belongs to the Special Issue Host-Parasite Relationships in Veterinary Parasitology: Get to Know Your Enemy before Fighting it)
Simple Summary
Fasciolid flukes collected from sheep and cattle in Ecuador showed a high diversity in DNA sequences whose analyses indicated introductions from South America, European and North American countries. These results agree with the numerous livestock importations performed by Ecuador. Abnormally big-sized liver flukes were found in Ecuadorian sheep. The morphometric phenotypic CIAS study showed that its size maximum and mean very pronouncedly and significantly surpassed those of the Fasciola hepatica populations from South America and Spain and proved to be intermediate between standard F. hepatica and F. gigantica populations. Such a feature is only known in intermediate fasciolid forms in Old World areas where the two species and their specific lymnaeid snail vectors overlap. This argues about a past hybridization after F. gigantica importation from Pakistan and/or introduction of intermediate hybrids previously generated in USA. The lack of heterozygotic rDNA ITS positions differentiating the two species, and of introgressed fragments and heteroplasmic positions in mtDNA genes, indicate a post-hybridization period sufficiently long as for rDNA concerted evolution to complete homogenization and mtDNA to return to homoplasmy. The vector specificity filter due to Radix absence should act as a driving force in accelerating such lineage evolution. Public health implications are finally emphasized.
Abstract
Fascioliasis is a disease caused by Fasciola hepatica worldwide transmitted by lymnaeid snails mainly of the Galba/Fossaria group and F. gigantica restricted to parts of Africa and Asia and transmitted by Radix lymnaeids. Concern has recently risen regarding the high pathogenicity and human infection capacity of F. gigantica. Abnormally big-sized fasciolids were found infecting sheep in Ecuador, the only South American country where F. gigantica has been reported. Their phenotypic comparison with F. hepatica infecting sheep from Peru, Bolivia and Spain, and F. gigantica from Egypt and Vietnam demonstrated the Ecuadorian fasciolids to have size-linked parameters of F. gigantica. Genotyping of these big-sized fasciolids by rDNA ITS-2 and ITS-1 and mtDNA cox1 and nad1 and their comparison with other countries proved the big-sized fasciolids to belong to F. hepatica. Neither heterozygotic ITS position differentiated the two species, and no introgressed fragments and heteroplasmic positions in mtDNA were found. The haplotype diversity indicates introductions mainly from other South American countries, Europe and North America. Big-sized fasciolids from Ecuador and USA are considered to be consequences of F.gigantica introductions by past livestock importations. The vector specificity filter due to Radix absence should act as driving force in the evolution in such lineages.
