Host defense or parasite cue: Skin secretions mediate interactions between amphibians and their parasites

Abstract

Amphibian skin secretions (substances produced by the amphibian plus microbiota) plausibly act as a first line of defense against pathogen attack, but may also provide chemical cues for pathogens. To clarify the role of skin secretions in host-parasite interactions, we conducted experiments using cane toads (Rhinella marina) and their lungworms (Rhabdias pseudosphaerocephala) from the range-core and invasion-front of the introduced anurans’ range in Australia. Depending on the geographic area, toad skin secretions can reduce the longevity and infection success of parasite larvae, or attract lungworm larvae and enhance their infection success. These striking differences between the two regions were due both to differential responses of the larvae, and differential effects of the skin secretions. Our data suggest that skin secretions play an important role in host-parasite interactions in anurans, and that the arms race between a host and parasite can rapidly generate spatial variation in critical features of that interaction.

In an arms race between host and parasite, a lungworm’s ability to infect a toad is determined by host susceptibility, not parasite preference

“…Changes in the evolved interaction between toads and their lungworm parasites appear to have been especially rapid at the toad invasion's range-edge in WA (7,29), likely because low population densities of hosts (toads) at the invasion front decrease rates of parasite transmission (27). As a result, selection for mounting an effective immune response to fight parasite attack may be weaker at the invasion front than elsewhere (consistent with the enemy release hypothesis: (45).…”

“…An arms-race has developed between toads and lungworms (27), resulting in toads from different parts of the invasive range having differential resistance to infection (30). Potential explanations for that spatial variation in vulnerability include differential skin permeability (28), attractiveness to lungworm larvae (29), or investment in immune responses (30) in toads from different areas. This system presents a robust opportunity to tease apart adaptations and the parasite versus its host in driving divergence in infectivity during an arms-race.…”

In an arms race between host and parasite, a lungworm's ability to infect a toad is determined by host susceptibility not parasite preference

“…Changes in the evolved interaction between toads and their lungworm parasites appear to have been especially rapid at the toad invasion's range-edge in WA [7,29], likely because of low population densities of hosts (toads) at the invasion front decrease rates of parasite transmission [27]. As a result, selection for mounting an effective immune response to fight parasite attack may be weaker at the invasion front than elsewhere (consistent with the enemy release hypothesis [46]).…”

“…An arms race has developed between toads and lungworms [27]. Range-front toads reduce investment in immune defences [28] but can be more resistant to infection from lungworms [7,29]. Potential explanations for that spatial variation in vulnerability include differential skin permeability [30], attractiveness to lungworm larvae [29] or investment in immune responses [28] in toads from different areas.…”

“…Range-front toads reduce investment in immune defences [28] but can be more resistant to infection from lungworms [7,29]. Potential explanations for that spatial variation in vulnerability include differential skin permeability [30], attractiveness to lungworm larvae [29] or investment in immune responses [28] in toads from different areas. This system presents a robust opportunity to tease apart adaptations and the parasite versus its host in driving divergence in infectivity during an arms race.…”