Paternal leakage and mtDNA heteroplasmy in Rhipicephalus spp. ticks

Valentina Mastrantonio,Antonio Parisi,Domenico Otranto,Roberta Iatta,Daniele Porretta,Maria Stefania Latrofa,Riccardo Paolo Lia,Filipe Dantas-Torres,Sandra Urbanelli

doi:10.1038/s41598-018-38001-8

Abstract

Paternal leakage of mitochondrial DNA (mtDNA) and heteroplasmy have been recently described in several animal species. In arthropods, by searching in the Scopus database, we found only 23 documented cases of paternal leakage. Therefore, although arthropods represent a large fraction of animal biodiversity, this phenomenon has been investigated only in a paucity of species in this phylum, thus preventing a reliable estimate of its frequency. Here, we investigated the occurrence of paternal leakage and mtDNA heteroplasmy in ticks belonging to one of the most significant tick species complexes, the so-called Rhipicephalus sanguineussensu lato. By developing a multiplex allele-specific PCR assay targeting a fragment of the 12S rRNA ribosomal region of the mtDNA, we showed the occurrence of paternal leakage and mtDNA heteroplasmy in R. sanguineuss.l. ticks originated from experimental crosses, as well as in individuals collected from the field. Our results add a new evidence of paternal leakage in arthropods and document for the first time this phenomenon in ticks. Furthermore, they suggest the importance of using allele-specific assays when searching for paternal leakage and/or heteroplasmy, as standard sequencing methods may fail to detect the rare mtDNA molecules.

Highlights

Maternal inheritance of mitochondrial DNA (mtDNA) has been deemed as a rule in animal species and several stochastic and deterministic molecular mechanisms preventing the transmission of paternal mtDNA to the zygote have been described[6,7,8,9,10]
The occurrence of paternal leakage has been recently hypothesized in the brown dog ticks (Rhipicephalus sanguineus sensu lato), as crossbreeding experiments between two temperate lineages of R. sanguineus s.l., namely Rhipicephalus sp
The multiplex allele-specific PCR assay (MAS-PCR) was designed to amplify a mitochondrial fragment of the 12S rRNA of R. sp

Summary

Introduction

Maternal inheritance of mtDNA has been deemed as a rule in animal species and several stochastic and deterministic molecular mechanisms preventing the transmission of paternal mtDNA to the zygote have been described[6,7,8,9,10]. Furthemore, mtDNA leakage might be more frequent than currently observed because it is only detectable when the parental mtDNA genomes are so different to be recognized. As consequence, it appears to be more common in interspecific crosses, paternal leakage may be common after crosses between conspecific individuals belonging to genetically divergent lineages[10,11,13]. Arthropods represent a large fraction of animal biodiversity and include several species of ecological, socio-economical and medical-veterinary importance[15,16,17,18,19], to date the occurrence of paternal leakage and mtDNA heteroplasmy has been documented only in a paucity of species. The occurrence of heteroplasmy in R. sanguineus s.l. ticks was screened by a newly developed multiplex allele-specific PCR assay (MAS-PCR) targeting a fragment of the 12S rRNA ribosomal region in the mtDNA

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