Discovery of Mating in the Major African Livestock Pathogen Trypanosoma congolense

Abstract

The protozoan parasite, Trypanosoma congolense, is one of the most economically important pathogens of livestock in Africa and, through its impact on cattle health and productivity, has a significant effect on human health and well being. Despite the importance of this parasite our knowledge of some of the fundamental biological processes is limited. For example, it is unknown whether mating takes place. In this paper we have taken a population genetics based approach to address this question. The availability of genome sequence of the parasite allowed us to identify polymorphic microsatellite markers, which were used to genotype T. congolense isolates from livestock in a discrete geographical area of The Gambia. The data showed a high level of diversity with a large number of distinct genotypes, but a deficit in heterozygotes. Further analysis identified cryptic genetic subdivision into four sub-populations. In one of these, parasite genotypic diversity could only be explained by the occurrence of frequent mating in T. congolense. These data are completely inconsistent with previous suggestions that the parasite expands asexually in the absence of mating. The discovery of mating in this species of trypanosome has significant consequences for the spread of critical traits, such as drug resistance, as well as for fundamental aspects of the biology and epidemiology of this neglected but economically important pathogen.

Congopain genes diverged to become specific to Savannah, Forest and Kilifi subgroups of Trypanosoma congolense, and are valuable for diagnosis, genotyping and phylogenetic inferences

“…Differences in the ability to recombine may account for the higher diversity within Savannah. Microsatellite analyses suggested high variability, most likely resulting from mating in Savannah (Morrison et al, 2009), and low genetic variability and predominant clonal reproduction in Forest (Simo et al, 2013). Compared with data from T. congolense, there is a limited polymorphism in CATL-like genes from T. brucei ssp.…”

“…In addition, at least one sequence from each of the SAV1 and SAV2 groups also appears to be derived from recombination events (indicated by 4 methods) (supplementary Fig.2). Although preliminary, these findings suggest that recombination may be an important process in generating the diverse repertoire of CP sequences within the Savannah subgroup, providing additional insights to the mating capability of this subgroup (Morrison et al, 2009).…”

Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species

“…Nevertheless, as a result of compositional differences, the scale of recombination varies between species, being more frequent among T. brucei and T. congolense VSG than in T. vivax, and more prevalent among T. brucei VSG than in T. congolense. Opportunities for allelic recombination among VSG may be affected by species differences in mating system; recent work indicates that sexual reproduction is frequent in T. brucei and T. congolense populations (28)(29), whereas T. vivax population structure is consistent with clonal reproduction (30). However, the importance of allelic recombination to VSG diversity is debatable; because the subtelomeres of homologous chromosomes in T. brucei are frequently dissimilar, subtelomeric VSG are effectively hemizygous, and so most recombination between VSG is ectopic (11).…”

Reproductive clonality of pathogens: A perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa

“…We have repeatedly considered selfing/strong homogamy as particular cases of clonality (2,3,123,161,190,193,194) and not as distinct evolutionary processes, a consideration shared by authors dealing with fungi (88,205,211) and parasitic protozoa (95,96,99,109,119,121,124,130,133,135,137,139,142,148). Other authors, mainly working with Leishmania species (107,111,115,116,212) but also with T. cruzi (153) and fungi (87,197), assert, however, that clonality should be distinguished from selfing/ inbreeding and that clonality should be limited to "strict" clonality, that is, mitotic propagation.…”

“…This restricted meaning is a matter of definition. Our opinion is that the broader definition of clonality, proposed by us and shared by most authors, which includes selfing/ homogamy, should be privileged for several reasons: (i) The evolutionary consequences of strict clonality and strong selfing/ homogamy are similar, in that they lead to linkage disequilibrium (LD) and the propagation of unchanged MLGs; (ii) restrained recombination is the important consideration in applied research, such as molecular epidemiology (strain tracking and typing) and tracing of genes of interest; (iii) although homogamy/selfing occurs in bacteria (51,58,199,200,213) and probably in viruses, most authors do not distinguish it from clonality; indeed, in the case of haploid organisms, the distinction is not relevant; (iv) most importantly, the population genetic means for distinguishing strict clonality from selfing/homogamy are questionable, because they rely on segregation tests designed mainly for diploid metazoa (107,111,115,116,148,195,197,208,209,212,214,215). The common observation is a deficit of heterozygotes, although it is argued that strict clonality (mitotic propagation) should lead to an excess, not a deficit of heterozygosity.…”