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. 2019 May 20;13(5):e0007392.
doi: 10.1371/journal.pntd.0007392. eCollection 2019 May.

Sexual reproduction in a natural Trypanosoma cruzi population

Affiliations

Sexual reproduction in a natural Trypanosoma cruzi population

Alexander S F Berry et al. PLoS Negl Trop Dis. .

Abstract

Background: Sexual reproduction provides an evolutionary advantageous mechanism that combines favorable mutations that have arisen in separate lineages into the same individual. This advantage is especially pronounced in microparasites as allelic reassortment among individuals caused by sexual reproduction promotes allelic diversity at immune evasion genes within individuals which is often essential to evade host immune systems. Despite these advantages, many eukaryotic microparasites exhibit highly-clonal population structures suggesting that genetic exchange through sexual reproduction is rare. Evidence supporting clonality is particularly convincing in the causative agent of Chagas disease, Trypanosoma cruzi, despite equally convincing evidence of the capacity to engage in sexual reproduction.

Methodology/ principle findings: In the present study, we investigated two hypotheses that can reconcile the apparent contradiction between the observed clonal population structure and the capacity to engage in sexual reproduction by analyzing the genome sequences of 123 T. cruzi isolates from a natural population in Arequipa, Peru. The distribution of polymorphic markers within and among isolates provides clear evidence of the occurrence of sexual reproduction. Large genetic segments are rearranged among chromosomes due to crossing over during meiosis leading to a decay in the genetic linkage among polymorphic markers compared to the expectations from a purely asexually-reproducing population. Nevertheless, the population structure appears clonal due to a high level of inbreeding during sexual reproduction which increases homozygosity, and thus reduces diversity, within each inbreeding lineage.

Conclusions/ significance: These results effectively reconcile the apparent contradiction by demonstrating that the clonal population structure is derived not from infrequent sex in natural populations but from high levels of inbreeding. We discuss epidemiological consequences of this reproductive strategy on genome evolution, population structure, and phenotypic diversity of this medically important parasite.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Reproductive strategies can be inferred from the distribution of polymorphic markers within and among strains in a population.
Both asexual and sexual populations experience both A) point mutations and B) gene conversion events while only populations reproducing sexually experience C) meiotic recombination that reassort large genomic regions among chromosomes as well as chromosomes among individuals. A) Point mutations alter random bases individually such that spatial clustering of mutations is not expected in most cases. Whole chromosomes carrying novel point mutations, along with all linked markers, will be passed to offspring during asexual reproduction. These markers can disassociate due to cross-over events and independent assortment of chromosomes during meiosis and sexual reproduction. B) Gene conversion events homogenize small regions of homologous chromosomes (<10kb), effectively reducing diversity at multiple markers in one chromosomal region. C) Sexual reproduction can result in the disassociation of polymorphic markers due to the independent assortment of chromosomes as well as crossing over between homologous chromosomes during meiosis. Crossing over results in the exchange of large chromosomal segments (up to Mbs) among homologous chromosomes, disrupting associations among polymorphic markers on each chromosome. Crossing over thus results in gametes that contain chromosomes comprised of a set of polymorphic sites derived from the one parental chromosome and a set derived from the other parental chromosome. As only a small number of cross-over events are expected to occur on each chromosome during meiosis (~1), a small number of large genomic regions reassort on each resulting chromosome, a genetic signature that is distinct from point mutations and gene conversion. Random fusion of gametes with these recombined chromosomes will produce offspring with some chromosomal regions that are uniformly homozygous at polymorphic markers which are heterozygous in their siblings.
Fig 2
Fig 2. Geographic distribution of isolates.
The location of all 123 sampled T. cruzi are represented by dots and colored by the host species. Inset shows the location of Arequipa. Map of Arequipa was obtained from https://landlook.usgs.gov and was modified using QGIS v. 2.18 [69]. Inset was modified from https://commons.wikimedia.org/wiki/Atlas_of_the_world.
Fig 3
Fig 3. The distribution of polymorphic markers within and among individuals provides clear evidence of meiotic recombination.
This representative subset of the data portrays the distributions of 325 polymorphic markers throughout three regions of the genome in 54 isolates (grouped by geographic location: Mariano Melgar Blocks 1–4 (N = 14), Block 5 (N = 11), Block 7 (N = 14), La Joya (N = 14), and Bustamante (N = 1)) that indicate the presence of sexual reproduction as A) the independent assortment of chromosomes among individuals in a population; B) meiotic recombination events that reassort polymorphic markers along a chromosome; and C) evidence of very recent reassortment of polymorphic markers via sexual reproduction. Markers that are polymorphic in the population can be heterozygous (green) or homozygous in each individual (yellow representing a site that is homozygous for one base, blue representing individuals homozygous for the alternative base). For clarity, only polymorphic sites with a minor allele frequency>16% in the population are shown here. (A) Independent assortment of chromosomes and subsequent fusion of gametes has resulted in a region (I) that is homozygous in some individuals and heterozygous in others across a 200kb region containing 128 polymorphic markers on an 829kb contig. In this region, individuals can be homozygous for either set of linked polymorphic markers. Interestingly, genotypes are geographically clustered, indicating identity by descent. Runs of identical color indicate identical sequence. (B) Meiotic recombination has resulted in a region (II) of a 357kb contig that partially retain the linkage patterns of both parental chromosomes while the rest retains the linkage pattern of only one parental chromosome, showing how crossing over can affect parts of chromosomes. In this region, there is evidence of at least three independent meiotic recombination events. (C) Sexual reproduction after a recent colonization of a city block has resulted in the genetic divergence of closely related samples over a run of polymorphic markers. For example, a meiotic recombination event is apparent in region II in one sampled individual on Block 7. The remaining contigs (S1 Fig) contain near-complete sequence similarity among all clones isolated from Block 7 suggesting that all individuals on this block share a recent common ancestor and the meiotic event occurring in region II occurred after the Block 7 was colonized. Similarly, a meiotic recombination event in a region (III) of a 130kb contig occurred in one lineage inhabiting Blocks 1–3 in Mariano Melgar. The regions shown here contain only some of the 474 meiotic recombination events distributed across 151 contigs, with each detected meiotic recombination event spanning from 10kb to nearly 500kb. The relative positions of each contig within the genome are unknown. For data spanning the whole genome, see S1 Fig.
Fig 4
Fig 4. Inbreeding results in a decay of heterozygosity.
After one generation of inbreeding, half of the offspring retain the heterozygosity found in the parent while half become homozygous. As diversity cannot be restored in homozygous regions in the absence of outcrossing and heterozygosity decays by half each generation, population-level heterozygosity continually declines in inbreeding populations until all lineages are homozygous.

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