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Models in parasite and pathogen evolution:

Genomic analysis reveals predominant clonality and progressive evolution at all evolutionary scales in parasitic protozoa, yeasts and bacteria


Michel Tibayrenc and Francisco J. Ayala

Maladies Infectieuses et Vecteurs Écologie, Génétique, Évolution et Contrôle, MIVEGEC (IRD 224-CNRS 5290-UM1-UM2), Institut de recherche pour le développement, Montpellier Cedex 5, France

Catedra Francisco Jose Ayala of Science, Technology, and Religion, University of Comillas, Madrid, Spain Locke Court, Irvine, CA, United States


Corresponding author: e-mail address: michel.tibayrenc@ird.fr


Contents

1. The predominant clonal evolution model: A brief recall 2

2. Growing affirmations from genomics 4

3. Parasitic protozoa 5

4. Yeast 15

5. Bacteria 16

6. Counterexamples 23

7. Discussion 26

Acknowledgements 31

Glossary 31

References 35


Abstract

The predominant clonal evolution (PCE) model of pathogenic microorganisms postulates

that the impact of genetic recombination in those pathogens’ natural populations

is not enough to erase a persistent phylogenetic signal at all evolutionary scales from

microevolution till geological times in the whole ecogeographical range of the species

considered. We have tested this model with a set of representative parasitic protozoa,

yeasts and bacteria in the light of the most recent genomic data. All surveyed species,

including those that were considered as highly recombining, exhibit similar PCE patterns

above and under the species level, from macro- to micro-evolutionary scales (Russian doll pattern), suggesting gradual evolution. To our knowledge, it is the first time that such a strong common evolutionary feature among very diverse pathogens has been evidenced. The implications of this model for basic biology and applied research are exposed. These implications include our knowledge on the pathogens’ reproductive mode, their population structure, the possibility to type strain and to follow up epidemics (molecular epidemiology) and to revisit pathogens’ taxonomy through a flexible use of the phylogenetic species concept.


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Fig. 1. A typical Russian doll pattern (RDP) in the species Leishmania infantum. Left: a phylogenetic tree of the whole “Leishmania donovani/infantum complex”, designed after MLEE analysis (after fig. 1 in Pratlong et al., 2013). Right: the multilocus genotype “MON-1”, which is a tiny part of the L. infantum species (left) proves to be highly heterogeneous and structured when analysed by microsatellites, which have a higher discriminatory power than MLEE (after fig. 2 in Kuhls et al., 2008).

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