Experimental evolution of Plasmodium yoelii in single and helminth-coinfected mice

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Abstract Coinfection has the potential to affect key traits describing the infection dynamics, the severity of the disease and in fine parasite fitness. However, despite its pervasiveness, experimental work investigating how parasites adapt to the conditions provided by a coinfected host is mostly missing. Here, we adopted an experimental evolution approach to investigate if coinfection with the nematode Heligmosomoides polygyrus (Hp) affected the infection dynamics and virulence of the murine malaria parasite Plasmodium yoelii (Py). To this purpose, lines of Py were passaged either in single infected hosts (SI-lines) or in hosts that had been previously infected with Hp (COI-lines). After five and seven passages, the infection dynamics and virulence of evolved lines were compared to the ancestral Py population during single infection trials. As expected, we found that serial passages increased parasitemia and Py virulence, due to the competitive advantage of genotypes with the fastest replication rate, but SI-lines and COI-lines had similar replication rate and virulence. Hosts infected with evolved lines of Py were also less tolerant (steeper slope between red blood cell counts and parasitemia) but again there was no difference between SI-lines and COI-lines. In a second experiment, COI-lines were also used to infect hosts during coinfection trials, allowing us to compare within-host Py replication when the environment during the evaluation trials matched the environment experienced during the passages and when they were mismatched. The results showed that COI-lines used during single infection trials (mismatched environment) had a slower replication rate compared to both SI-lines and COI-lines used during matched-environment trials. Overall, although we did not find any difference in the virulence of SI-lines and COI-lines after seven passages, Py rapidly adapted to the environmental conditions provided by single infected or coinfected hosts, as shown by the slower replication rate found in mismatched-environment trials. Author Summary Coinfection can alter infection dynamics, disease severity, and parasite fitness, yet experimental evidence on parasite adaptation to coinfected hosts is scarce. Here we used experimental evolution to assess whether coinfection with the nematode Heligmosomoides polygyrus influences the infection dynamics and virulence of the murine malaria parasite Plasmodium yoelii . Parasite lines were serially passaged in either single infected hosts or hosts previously infected with Heligmosomoides polygyrus . After multiple passages, evolved lines exhibited increased parasitemia and virulence compared to the ancestral strain, but no significant differences were found between lines evolved in single or coinfected hosts. Notably, parasite replication was reduced when lines evolved in coinfected hosts were tested in single infection environments, indicating rapid adaptation to host infection context. This suggests that while coinfection shapes within-host conditions, Plasmodium adapts rapidly to these conditions. These results have possible implications for understanding parasite evolution in fluctuating host environments, and the microevolutionary consequences for malaria of the deworming campaigns that are implemented to control helminthiases.

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