Infection sequence alters disease severity—Effects of the sequential exposure of two larval trematodes to Polypedates cruciger tadpoles

Abstract

Multiple pathogens coexist in nature, and hence, host species often encounter several pathogens simultaneously. The sequence in which the host encounters the parasites influences interactions between parasites and host pathology. Here, the effects of infection by two cercaria (larvae of trematodes) types, pleurolophocercous cercaria of Acanthostomum burminis and a furcocercous cercaria, on the tadpoles of common hourglass tree frog (Polypedates cruciger) were examined. Ten days posthatch, tadpoles (Gosner stage 27/28) were used for infection exposures. First, in a single infection each cercaria type was introduced to the tadpoles separately. Second, coinfection of the two cercaria was carried out by alternating the sequences of exposure. For all the experiments, appropriate controls were instituted. Tadpoles of all groups exposed to parasites had lower survival levels compared to controls. Among the four groups exposed, the highest survival was observed in the coinfection when furcocercous was introduced first (82.5%). The lowest survival was observed in the coinfection when the A. burminis cercaria was introduced first (65.0%). In the coinfections, when A. burminis was introduced prior to furcocercous, survival of the tadpoles was reduced by 17.0% compared to the exposures of furcocercous prior to A. burminis. Prior infection with A. burminis induced negative effect on the host with an increased infection severity, while prior infection with furcocercous had reduced infection severity than lone exposures. These results suggest that furcocercous infections can be beneficial for hosts challenged with A. burminis provided that A. burminis exposure occurs second. None of the treatments had an effect on the growth of the tadpoles, but lengthening of developmental period was observed in some exposures. All exposed tadpoles developed malformations which were exclusively axial—kyphosis and scoliosis. However, there was no difference in the number of malformed individuals in the single infection (19.0%–25.0%) compared to coinfection (20.0%–22.5%) or between coinfections. The results suggest that the sequence of parasite exposure affects host–parasite interactions and hence the disease outcomes. Understanding the effects of coinfection on disease outcomes for hosts provides insight into disease dynamics.

Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

“…Although there are many records of abnormal amphibians in Eurasia [1], only some cases of trematode-dependent anomalies were strongly supported by laboratory experiments [20][21][22][23][24][25]. Here, we describe new variants of morphological anomalies caused by the trematode Strigea robusta in Eurasian amphibians.…”

“…Recent studies have shown that, in several amphibian species, the anomalies can be caused by some species of trematodes [13][14][15][16][17][18][19][20][21][22][23][24][25]. The most investigated cases concerned the trematode Ribeiroia ondatrae in many amphibian populations across the USA and Canada [13][14][15].…”

Higher-order interactions among coinfecting parasites and a microbial mutualist impact disease progression

“…Further, the magnitude of this facilitation depended on infection sequence. There is growing evidence that infection sequence can determine the magnitude and direction of the effect of within-host microbial interactions [42,44,45].…”

“…The direction and magnitude of interactions among parasites and hostassociated microbiota may depend on the sequence in which they infect host individuals [41][42][43][44][45]. While simultaneous coinfections can occur in nature [46], more often, microbes infect a host at different time points [41].…”

Immune Digital Twin Blueprint: A Comprehensive Mechanistic Model of the Human Immune System

“…The importance of infection order has been discussed in the case of the parasite coinfections (35) . Recently, it was shown that the sequence of larval trematodes in tadpoles could also affect the disease severity (36) . In a different in vitro study in swine alveolar macrophages, the infection order of porcine circovirus type 2 and porcine reproductive and respiratory syndrome virus affected the cytokine response (37) .…”