Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning

Fascioliasis causes high economic losses in livestock and underlies public health problems in rural areas, mainly of low-income countries. The increasing animal infection rates in Bangladesh were assessed, by focusing on host species, different parts of the country, and rDNA sequences. Fasciolid flu...

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Main Authors: Syed Ali Ahasan, Alejandra De Elías-Escribano, Patricio Artigas, Mohammad Zahangir Alam, M. Motahar Hussain Mondal, David Blair, Emdadul Haque Chowdhury, M. Dolores Bargues, Santiago Mas-Coma
Format: Article
Language:English
Published: Elsevier 2023-12-01
Series:One Health
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352771423001349
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author Syed Ali Ahasan
Alejandra De Elías-Escribano
Patricio Artigas
Mohammad Zahangir Alam
M. Motahar Hussain Mondal
David Blair
Emdadul Haque Chowdhury
M. Dolores Bargues
Santiago Mas-Coma
author_facet Syed Ali Ahasan
Alejandra De Elías-Escribano
Patricio Artigas
Mohammad Zahangir Alam
M. Motahar Hussain Mondal
David Blair
Emdadul Haque Chowdhury
M. Dolores Bargues
Santiago Mas-Coma
author_sort Syed Ali Ahasan
collection DOAJ
description Fascioliasis causes high economic losses in livestock and underlies public health problems in rural areas, mainly of low-income countries. The increasing animal infection rates in Bangladesh were assessed, by focusing on host species, different parts of the country, and rDNA sequences. Fasciolid flukes were collected from buffaloes, cattle, goats and sheep from many localities to assess prevalences and intensities of infection. The nuclear rDNA internal transcribed spacer (ITS) region including ITS-1 and ITS-2 spacers was analyzed by direct sequencing and cloning, given the detection of intermediate phenotypic forms in Bangladesh. The 35.4% prevalence in goats and 55.5% in buffaloes are the highest recorded in these animals in Bangladesh. In cattle (29.3%) and sheep (26.8%) prevalences are also high for these species. These prevalences are very high when compared to lowlands at similar latitudes in neighboring India. The high prevalences and intensities appear in western Bangladesh where cross-border importation of animals from India occur. The combined haplotype CH3A of Fasciola gigantica widely found in all livestock species throughout Bangladesh fits its historical connections with the western Grand Trunk Road and the eastern Tea-Horse Road. The “pure” F. hepatica sequences only in clones from specimens showing heterozygotic positions indicate recent hybridization events with local “pure” F. gigantica, since concerted evolution did not yet have sufficient time to homogenize the rDNA operon. The detection of up to six different sequences coexisting in the cloned specimens evidences crossbreeding between hybrid parents, indicating repeated, superimposed and rapidly evolving hybridization events. The high proportion of hybrids highlights an increasing animal infection trend and human infection risk, and the need for control measures, mainly concerning goats in household farming management. ITS-1 and ITS-2 markers prove to be useful for detecting recent hybrid fasciolids. The introduction of a Fasciola species with imported livestock into a highly prevalent area of the other Fasciola species may lead to a high nucleotide variation in the species-differing positions in the extremely conserved fasciolid spacers. Results suggest that, in ancient times, frequent crossbreeding inside the same Fasciola species gave rise to the very peculiar characteristics of the present-day nuclear genome of both fasciolids.
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spelling doaj.art-79c7cc2313024380b3f2fd7e78f1117e2023-12-12T04:35:09ZengElsevierOne Health2352-77142023-12-0117100614Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloningSyed Ali Ahasan0Alejandra De Elías-Escribano1Patricio Artigas2Mohammad Zahangir Alam3M. Motahar Hussain Mondal4David Blair5Emdadul Haque Chowdhury6M. Dolores Bargues7Santiago Mas-Coma8Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain; Department of Pathology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh; Department of Livestock Services, Dhaka, BangladeshDepartamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain; CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, C/ Monforte de Lemos 3-5, Pabellón 11, Planta 0, 28029 Madrid, SpainDepartamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain; CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, C/ Monforte de Lemos 3-5, Pabellón 11, Planta 0, 28029 Madrid, SpainDepartment of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, BangladeshDepartment of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, BangladeshCollege of Science and Engineering, James Cook University, James Cook Dr 1, Townsville 4814, Queensland, AustraliaDepartment of Pathology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh; Department of Livestock Services, Dhaka, BangladeshDepartamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain; CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, C/ Monforte de Lemos 3-5, Pabellón 11, Planta 0, 28029 Madrid, Spain; Corresponding author at: Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain.Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain; CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, C/ Monforte de Lemos 3-5, Pabellón 11, Planta 0, 28029 Madrid, SpainFascioliasis causes high economic losses in livestock and underlies public health problems in rural areas, mainly of low-income countries. The increasing animal infection rates in Bangladesh were assessed, by focusing on host species, different parts of the country, and rDNA sequences. Fasciolid flukes were collected from buffaloes, cattle, goats and sheep from many localities to assess prevalences and intensities of infection. The nuclear rDNA internal transcribed spacer (ITS) region including ITS-1 and ITS-2 spacers was analyzed by direct sequencing and cloning, given the detection of intermediate phenotypic forms in Bangladesh. The 35.4% prevalence in goats and 55.5% in buffaloes are the highest recorded in these animals in Bangladesh. In cattle (29.3%) and sheep (26.8%) prevalences are also high for these species. These prevalences are very high when compared to lowlands at similar latitudes in neighboring India. The high prevalences and intensities appear in western Bangladesh where cross-border importation of animals from India occur. The combined haplotype CH3A of Fasciola gigantica widely found in all livestock species throughout Bangladesh fits its historical connections with the western Grand Trunk Road and the eastern Tea-Horse Road. The “pure” F. hepatica sequences only in clones from specimens showing heterozygotic positions indicate recent hybridization events with local “pure” F. gigantica, since concerted evolution did not yet have sufficient time to homogenize the rDNA operon. The detection of up to six different sequences coexisting in the cloned specimens evidences crossbreeding between hybrid parents, indicating repeated, superimposed and rapidly evolving hybridization events. The high proportion of hybrids highlights an increasing animal infection trend and human infection risk, and the need for control measures, mainly concerning goats in household farming management. ITS-1 and ITS-2 markers prove to be useful for detecting recent hybrid fasciolids. The introduction of a Fasciola species with imported livestock into a highly prevalent area of the other Fasciola species may lead to a high nucleotide variation in the species-differing positions in the extremely conserved fasciolid spacers. Results suggest that, in ancient times, frequent crossbreeding inside the same Fasciola species gave rise to the very peculiar characteristics of the present-day nuclear genome of both fasciolids.http://www.sciencedirect.com/science/article/pii/S2352771423001349Fasciola gigantica and F. hepaticaLivestockPrevalences and intensitiesNuclear rDNA internal transcribed spacer regionITS-1 and ITS-2Sequencing and cloning
spellingShingle Syed Ali Ahasan
Alejandra De Elías-Escribano
Patricio Artigas
Mohammad Zahangir Alam
M. Motahar Hussain Mondal
David Blair
Emdadul Haque Chowdhury
M. Dolores Bargues
Santiago Mas-Coma
Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
One Health
Fasciola gigantica and F. hepatica
Livestock
Prevalences and intensities
Nuclear rDNA internal transcribed spacer region
ITS-1 and ITS-2
Sequencing and cloning
title Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
title_full Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
title_fullStr Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
title_full_unstemmed Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
title_short Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning
title_sort wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in bangladesh assessed by rdna internal transcribed spacer region sequencing and cloning
topic Fasciola gigantica and F. hepatica
Livestock
Prevalences and intensities
Nuclear rDNA internal transcribed spacer region
ITS-1 and ITS-2
Sequencing and cloning
url http://www.sciencedirect.com/science/article/pii/S2352771423001349
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