The Adaptive Host Manipulation Hypothesis: Parasites Modify the Behaviour, Morphology, and Physiology of Amphibians

Abstract

Parasites have evolved different strategies to increase their transmission from one host to another. The Adaptive Host Manipulation hypothesis states that parasites induce modifications of host phenotypes that could maximise parasite fitness. There are numerous examples of parasite manipulation across a wide range of host and parasite taxa. However, the number of studies exploring the manipulative effects of parasites on amphibians is still scarce. Herein, we extensively review the current knowledge on phenotypic alterations in amphibians following parasite infection. Outcomes from different studies show that parasites may manipulate amphibian behaviours to favour their transmission among conspecifics or to enhance the predation of infected amphibians by a suitable definite host. In addition, parasites also modify the limb morphology and impair locomotor activity of infected toads, frogs, and salamanders, hence facilitating their ingestion by a final host and completing the parasite life cycle. Additionally, parasites may alter host physiology to enhance pathogen proliferation, survival, and transmission. We examined the intrinsic (hosts traits) and extrinsic (natural and anthropogenic events) factors that may determine the outcome of infection, where human-induced changes of environmental conditions are the most harmful stressors that enhance amphibian exposure and susceptibility to parasites.

Juvenile agile frogs spatially avoid ranavirus-infected conspecifics, but do not show generalized social distancing or self-isolation

“…Such manipulation by the pathogen to facilitate its transmission is well-known from many hostpathogen systems (Klein 2003;Hernandez-Caballero et al 2022). Besides other pathogens, viruses are also known to be able to modify the behaviour of their hosts to their advantage (Goulson 1997;Hanlon 2013).…”

“…In our study system, in the case of infected focal individuals, the observed increase in spatial proximity to the healthy conspecific might not necessarily result from avoidance of the infected stimulus but may be the manifestation of the pathogen manipulating the hosts’ behaviour: infection with Rv may have driven froglets to stay close to non-infected conspecifics. Such manipulation by the pathogen to facilitate its transmission is well-known from many host-pathogen systems (Klein 2003; Hernandez-Caballero et al 2022). Besides other pathogens, viruses are also known to be able to modify the behaviour of their hosts to their advantage (Goulson 1997; Hanlon 2013).…”

Diversity of trematodes from the amphibian anomaly P hotspot: Role of planorbid snails

“…Deformities in amphibians caused by trematodes were detected under the effects of several trematode species: Ribeiroia ondatrae (Price, 1931) in North America, Acanthostomum burminis (Bhalerao, 1926) Bhalerao, 1936 in Sri-Lanka, Holostephanus volgensis (Sudarikov, 1962) Vojtkova, 1966 and Strigea robusta in Europe and Asia [33,37]. The most investigated variant is the Ribeiroia ondatrae infection in the North American amphibians [4,13,27,50,[113][114][115][116][117][118][119][120][121][122][123].…”

“…[22][23][24][30][31][32]. In Europe, several hotspots are known in which trematodes change the morphology of second intermediate hosts [33]. One of these cases is the anomaly P syndrome hotspot found in some populations of water frogs and toads.…”

“…One of these cases is the anomaly P syndrome hotspot found in some populations of water frogs and toads. The anomaly P includes various deformities of hindlimbs and forelimbs: i.e., flexion of hindlimbs, brachymely, polydactyly, various bone spines, tumor-like formation in inguinal region, and sometimes additional tiny limbs (Fig 1) in tadpoles and metamorphs [33][34][35][36]. The anomaly was found to be caused by the trematode Strigea robusta (Szidat, 1928) metacercariae [37].…”