New insights into the evolutionary history of Plasmodium falciparum from mitochondrial genome sequence analyses of Indian isolates

Abstract

Estimating genetic diversity and inferring the evolutionary history of Plasmodium falciparum could be helpful in understanding origin and spread of virulent and drug-resistant forms of the malaria pathogen and therefore contribute to malaria control programme. Genetic diversity of the whole mitochondrial (mt) genome of P. falciparum sampled across the major distribution ranges had been reported, but no Indian P. falciparum isolate had been analysed so far, even though India is highly endemic to P. falciparum malaria. We have sequenced the whole mt genome of 44 Indian field isolates and utilized published data set of 96 genome sequences to present global genetic diversity and to revisit the evolutionary history of P. falciparum. Indian P. falciparum presents high genetic diversity with several characteristics of ancestral populations and shares many of the genetic features with African and to some extent Papua New Guinean (PNG) isolates. Similar to African isolates, Indian P. falciparum populations have maintained high effective population size and undergone rapid expansion in the past with oldest time to the most recent common ancestor (TMRCA). Interestingly, one of the four single nucleotide polymorphisms (SNPs) that differentiates P. falciparum from P. falciparum-like isolates (infecting non-human primates in Africa) was found to be segregating in five Indian P. falciparum isolates. This SNP was in tight linkage with other two novel SNPs that were found exclusively in these five Indian isolates. The results on the mt genome sequence analyses of Indian isolates on the whole add to the current understanding on the evolutionary history of P. falciparum.

Mitochondrial DNA from the eradicated European Plasmodium vivax and P. falciparum from 70-year-old slides from the Ebro Delta in Spain

“…The obtained P. falciparum sequence and additional 698 mtDNA sequences (SI Materials and Methods) from different continents (11,13,33,34) were used to reconstruct a haplotype using the same methodology previously described with P. vivax.…”

“…Although some suggest that the pathogen followed the original Homo sapiens dispersals around 60,000 y ago (12), others support a recent expansion within the last 5,000-10,000 y associated to the advent of agriculture (2). The recent analysis of 44 Indian field isolates showed, however, a higher than expected diversity and suggested that the Indian strains are also part of the ancestral distribution range of P. falciparum (13). Historical accounts seem to indicate that malaria spread from India into the Mediterranean at the time of Classical Greece; therefore, the now extinct European P. falciparum could be genetically related to some of these Indian parasites.…”

Mitochondrial population genomic analyses reveal population structure and demography of Indian Plasmodium falciparum

“…However, a recent study including 44 mt genomes of Indian P. falciparum has indicated high prevalence of the central mt genome haplotype (H_5) both in India and Africa and ancient population expansion in these two places (Tyagi et al, 2014a). This proposition is substantiated by the fact that the observed genetic diversities found in Indian P. falciparum are comparable to that of African isolates (Tyagi et al, 2014a(Tyagi et al, , 2014b.…”

“…However, a recent study including 44 mt genomes of Indian P. falciparum has indicated high prevalence of the central mt genome haplotype (H_5) both in India and Africa and ancient population expansion in these two places (Tyagi et al, 2014a). This proposition is substantiated by the fact that the observed genetic diversities found in Indian P. falciparum are comparable to that of African isolates (Tyagi et al, 2014a(Tyagi et al, , 2014b. Furthermore, a recent study with the whole mt genome sequence analyses of 516 global P. falciparum isolates have also proposed African origin of P. falciparum (Tanabe et al, 2013) and the observed genetic differentiation between three major geographic regions/continents (Africa, Southeast Asia and Oceania) were generally found to be higher than that among populations within these continents (Tanabe et al, 2013) which corroborate the findings from population genetic studies of microsatellite polymorphisms in P. falciparum (Anderson et al, 2000).…”

“…The whole mt genome sequence diversities have been employed to understand the origin and demographic histories of P. falciparum (Conway et al, 2000;Joy et al, 2003;Tanabe et al, 2013). Furthermore, a very recent study comparing the whole mt genome sequence diversity in 44 Indian P. falciparum isolates with the published 96 sequences of global isolates have revisited the global evolutionary history of this species (Tyagi et al, 2014a). Such wide usage of the mt genome sequences has therefore proved their usability for inference of population evolutionary history of malaria parasites in general, and application of the knowledge in malaria epidemiology, in particular.…”