Genetic evidence for hybridisation between Haemonchus contortus and Haemonchus placei in natural field populations and its implications for interspecies transmission of anthelmintic resistance

• Published in: International journal for parasitology Vol. 45; no. 2-3; pp. 149 - 159
• Main Authors: Chaudhry, Umer, Redman, Elizabeth M., Abbas, Muhammad, Muthusamy, Raman, Ashraf, Kamran, Gilleard, John S.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.02.2015
• Subjects: Animals; Anthelmintic resistance; Anthelmintics - pharmacology; Co-infection; Crosses, Genetic; DNA, Helminth - chemistry; DNA, Helminth - genetics; DNA, Ribosomal Spacer - chemistry; DNA, Ribosomal Spacer - genetics; Drug Resistance; Genotype; Haemonchus - classification; Haemonchus - drug effects; Haemonchus - genetics; Haemonchus contortus; Haemonchus placei; Hybridisation; Hybridization, Genetic; India; Introgression; Mecistocirrus; Molecular Sequence Data; Pakistan; Ruminants - parasitology; Sequence Analysis, DNA; Pakistan; India; Haemonchus contortus; Mecistocirrus; Co-infection; Haemonchus placei; Anthelmintic resistance; Introgression; Hybridisation
• ISSN: 0020-7519; 1879-0135
• DOI: 10.1016/j.ijpara.2014.09.002

Hybridisation between Haemonchus species in the field. [Display omitted] •The most comprehensive genetic proof of F1 hybrids between two parasitic nematode species of humans or animals in the field.•Definitive demonstration is presented that hybridisation occurs between Haemonchus contortus and H. placei in the field.•New genetic markers were used to identify H. contortus, H. placei and hybrid worms.•Co-infection of H. contortus and H. placei is common in small ruminants from Pakistan.•Only H. contortus found in small ruminants from southern India. Genetic hybridisation between parasitic nematode species has potentially important consequences. It could lead to the introgression of genes between species including those involved in pathogenicity, host specificity, transmission and drug resistance. It could also complicate diagnosis and control. However, there are few compelling examples of its occurrence in parasites in the field. Haemonchus contortus and Haemonchus placei are two closely related parasitic nematode species that predominantly infect small ruminants and cattle, respectively. They are capable of experimental hybridisation when adult worms of each species are transplanted into the same individual host. Given that co-infection occurs in both small ruminants and cattle, there is potential for hybridisation in the field. However, this has not been definitively demonstrated and its extent is unknown. We investigated the occurrence of co-infection and interspecies hybridisation in H. contortus and H. placei in field populations from small ruminants from Pakistan and southern India using a number of independent genetic markers. Haemonchus contortus and H. placei co-infections were common in Pakistan but not in southern India where H. placei appeared to be absent in small ruminant hosts. In the former region, a number of worms were identified that were heterozygous for fixed, species-specific rDNA internal transcribed spacer 2 (ITS-2) single nucleotide polymorphisms. Genotyping of these ITS-2 heterozygotes with an additional four nuclear markers conclusively demonstrated them to be F1 interspecies hybrids. Mitochondrial NADH dehydrogenase subunit 4 haplotype analysis demonstrated that four of the hybrid worms had a H. placei maternal parent and one had a H. contortus maternal parent showing that hybridisation could occur in either direction. Interestingly, one of these hybrids contained an H. contortus isotype-1 β-tubulin benzimidazole resistance allele, suggesting there is a potential for interspecies introgression of drug resistance loci. We believe this is the first definitive genetic evidence of hybridisation between H. contortus and H. placei in the field and represents the most comprehensive genetic evidence of F1 hybrids between any human or livestock parasitic nematode species to date. Further, it suggests that interspecies transmission of anthelmintic resistance mutations warrants further investigation.