Discovery and genomic analyses of hybridization between divergent lineages of Trypanosoma congolense, causative agent of Animal African Trypanosomiasis

Abstract

Hybrid populations and introgressive hybridization remain poorly documented in pathogenic micro-organisms, as such that genetic exchange has been argued to play a minor role in their evolution. Recent work demonstrated the existence of hybrid microsatellite profiles in Trypanosoma congolense, a parasitic protozoan with detrimental effects on livestock productivity in sub-Saharan Africa. Here, we present the first population genomic study of T. congolense, revealing a remarkable number of single nucleotide polymorphisms (SNPs), small insertions/deletions (indels) and gene deletions among 56 parasite genomes from ten African countries. One group of parasites from Zambia was particularly diverse, displaying a substantial number of heterozygous SNP and indel sites compared to T. congolense parasites from the nine other sub-Saharan countries. Genomewide 5-kb phylogenetic analyses based on phased SNP data revealed that these parasites were the product of hybridization between phylogenetically distinct T. congolense lineages. Other parasites within the same region in Zambia presented a mosaic of haplotypic ancestry and genetic variability, indicating that hybrid parasites persisted and recombined beyond the initial hybridization event. Our observations challenge traditional views of trypanosome population biology and encourage future research on the role of hybridization in spreading genes for drug resistance, pathogenicity and virulence.

Mitonuclear genomics challenges the theory of clonality in Trypanosoma congolense: Reply to Tibayrenc and Ayala

“…Contrary to our conclusions, Tibayrenc and Ayala () stated that “the genomic data by Tihon et al. () as well as data from previous authors support the presence in this species of PCE features.” We are not sure which “previous authors” Tibayrenc and Ayala are referring to (see also concerns raised by Ramirez and Llewellyn () and Rougeron, De Meeûs, and Banuls () on the practice of self‐ and mis‐citation by Tibayrenc and Ayala). Perhaps the authors were referring to the work of Simo et al.…”

“…Our genomic data confirmed previous observations based on early enzyme analyses (e.g., Young & Godfrey, ) that Savannah and Forest parasites represent two discrete lineages (Tihon, Imamura, Dujardin, Van Den Abbeele, & Van den Broeck, ). Tibayrenc and Ayala () believe this observation supports PCE and they equate these lineages to near‐clades, namely a phylogenetic line that is clouded by occasional recombination.…”

“…(). Indeed, these are the only studies that (a) explored recombination within un‐subdivided populations in Savannah T. congolense (see also section 1) and (b) provided enough power to detect recombination, either through the analyses of a large number of samples (Morrison et al., ) or markers (Tihon et al., ). We believe it is important to shortly iterate the main findings of these studies as they challenge PCE:…”

Hybridization in Trypanosoma congolense does not challenge the predominant clonal evolution model. A comment on Tihon et al., 2017, Mol. Ecol.

“…In the study by Tihon et al. (), genomic data fully confirm (their figure 2) the individualization of Savannah vs. Forest (again congruence criterion).…”

Barcoding in trypanosomes

“…And, whilst there has been a drive to develop and refine new molecular diagnostics, the sensitivity of existing techniques may be greatly improved if more research was conducted on initial stages, such as sample preparation and DNA extraction (Dunlop et al 2014). However, recent developments in molecular methods for trypanosome identification have succeeded in unveiling a number of previously unidentified species (Adams et al 2010;Hutchinson and Gibson, 2015) and may offer new opportunities for the identification of novel hybrids (Koffi et al 2015;Tihon et al 2017) and the epidemiological tracking of trypanosome strains spread by the movement of host cattle (Févre et al 2005). Nonetheless, a lack of comparable data between parasite surveys makes it difficult to draw any firm conclusions regarding species prevalence, and the full extent of trypanosome diversity remains unknown at this time (Adams et al 2010;D'Avila-Levy et al 2015).…”