Rare but evolutionarily consequential outcrossing in a highly inbred zoonotic parasite

Authors: LA ROSA, GUISEPPE - Istituto Superiore Di Sanita; BERNAL, RAFAEL - Universidad De Extremadura; PEREZ MARTIN, J.E. - Universidad De Extremadura; TONANZI, D. - Istituto Superiore Di Sanita; SERRANO AGUILERA, F. - Universidad De Extremadura; Rosenthal, Benjamin; POZIO, EDOARDO - Istituto Superiore Di Sanita

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2017
Publication Date: 3/8/2018
Citation: La Rosa, G., Bernal, R., Perez Martin, J., Tonanzi, D., Serrano Aguilera, F., Rosenthal, B.M., Pozio, E. 2018. Rare but evolutionarily consequential outcrossing in a highly inbred zoonotic parasite. International Journal for Parasitology. https://doi.org/10.1016/j.ijpara.2017.12.007
DOI: https://doi.org/10.1016/j.ijpara.2017.12.007

Interpretive Summary: Combatting parasitic infection requires that we understand how uniform, or varied, they are. Will a single vaccine or medication suffice, or should differences in response be expected? The answer could depend on whether the parasite routinely engages in self-mating, or if genetic variants are widely shared among freely breeding individuals. We sought to understand the extent of inbreeding in Trichinella spiralis, a zoonotic parasite that occurs in a variety of animals and can be aquired by consuming undercooked meat. We found strong evidence for inbreeding in two-thirds of infected wild boar, but we found evidence that the remaining third posessed parasites from more than one pair of parents. The resulting outcrossing should limit distinctions that would otherwise accumulate among transmission chains. Conditions of transmission may differ in other regions, where such epidemiological features may engender different evolutionary outcomes. These results will interest veterinarians, parasitologists, epidemiologists, ecologists, and evolutionary biologists.

Technical Abstract: Recurrent self-mating can result in nearly clonal propagation of biological lineages, but even occasional outcrossing can serve to redistribute variation in future generations, providing cohesion among regional populations. The zoonotic parasite Trichinella spiralis has been suspected to undergo frequent inbreeding, resulting in genetically uniform larval cohorts which differ markedly from one another. Here, we explored the extent of inbreeding for this parasite by determining how genetic variation (at variable microsatellite markers) is distributed among 1,379 larvae derived from 41 wild boar in Extremadura, Spain. In particular, we sought to determine how much of the genetic variation in this region’s parasites occurs among the larvae of any given wild boar, and whether each derives from one, or more, parental lineages. We found strong evidence for inbreeding, resulting in genetically distinct parasite subpopulations among the parasites derived from many pairs of wild boar. Fully two-thirds of these parasite cohorts appear to derive from inbred parents; in ten percent of the wild boar, parasites were so inbred as to become absolutely fixed in all of the assayed genetic loci. In spite of this, more than one pair of parents appear to have given rise to the infections in one-third of the sampled wild boar, resulting in mixed infections. These mixed infections should slow the loss heterozygosity and the loss of multi-locus polymorphism in any given parasite lineage. Such outcrossing should limit distinctions that would otherwise accumulate among transmission chains, thereby enforcing cohesion through the region’s population in spite of its marked departure from panmixia. Conditions of transmission may differ in other regions, where such epidemiological features may engender different evolutionary outcomes.