Intraspecific variation in resistance of frog eggs to fungal infection

Abstract

Documenting sources of variation in host viability at pathogen exposure within and among populations is an important task in order to predict host-pathogen evolutionary dynamics. In the present study, we investigated family and population variation in the degree of embryonic infection of the pathogenic fungus Saprolegnia spp., by infecting moor frog (Rana arvalis) eggs from six populations and exposing them to two different temperatures. We found a significant family effect on the degree of Saprolegnia-infection of eggs and embryos, suggesting that there is genetic variation in resistance among embryos, or variation among females in some aspect of maternally induced resistance. Furthermore, infection level differed significantly between temperatures, with most families having more infected eggs in the relatively colder temperature. However, eggs and embryos from the different populations showed different degrees of Saprolegnia-infection in the two temperatures, i.e., there was a significant population · temperature interaction on the proportion of infected eggs. Thus, the degree of Saprolegnia-infection is sensitive to variation at the level of the family, population and environmental conditions, suggesting that responses to fungal outbreaks will vary geographically and will be difficult to predict.

A genetic component of resistance to fungal infection in frog embryos

“…Families (clutches) vary in their degree of infection to Saprolegnia in both toads and frogs Sagvik et al 2008). Our present results suggest that, in R. arvalis, maternal effects do not represent a major contribution to variation in infection of eggs and embryos as has previously been hypothesized (Sagvik et al 2008).…”

“…Thus, our data may instead suggest the presence of embryo-specific immunity (Hamdoun & Epel 2007). The nature of this proposed immune function is unknown but an active role of the developing embryo in preventing (rather than just escaping) fungal infection is supported by the observation that infertile eggs or dead embryos are more likely to be infected than live embryos (Kudo & Teshima 1991;Robinson et al 2003) and by an increased number of infected eggs from clutches with a higher degree of infertility, also in species with limited plasticity in developmental timing (Sagvik et al 2008;present study). Thus, females mated to males with low fertilizing ability may pay a twofold cost-in terms of both the number of offspring and an increased risk for the fertilized eggs to be infected by fungi (Moreira & Barata 2005), in particular under conditions generally promoting infection (e.g.…”

“…Although it cannot be completely discarded due to low levels of infection per jar, the low variation in time to hatching suggests that variation in the duration of embryonic development or developmental plasticity of growth rates under Saprolegnia infection is unlikely to explain our results (Sagvik et al 2008). Thus, our data may instead suggest the presence of embryo-specific immunity (Hamdoun & Epel 2007).…”

“…This should favour the evolution of maternal strategies (e.g. allocation of immunological factors in relation to perceived risk of infection; Grindstaff et al 2003) that limit or prevent fungal infection of developing embryos (Hamdoun & Epel 2007), suggesting that variation among families in susceptibility to fungal pathogens may be due to maternal effects (Sagvik et al 2008). However, variation in the degree of infection could also reflect genetic variation in embryo-specific immunity or offspring developmental plasticity in response to external threats to survival that do not rely upon maternal transfer of resources or information (Hamdoun & Epel 2007).…”

Water molds of the genera Saprolegnia and Leptolegnia are pathogenic to the North American frogs Rana catesbeiana and Pseudacris crucifer, respectively

“…For example, salamander adults are more susceptible to Saprolegnia parasitica in water polluted by motor oil (Lefcort et al 1997), and frog eggs are more susceptible to infection under exposure to ambient levels of UV-B radiation in shallow water (Kiesecker & Blaustein 1995, Kiesecker et al 2001b. Temperature also affects the susceptibility of amphibian eggs to infection (Ruthig 2006, 2008, Sagvik et al 2008b. Water molds are also important pathogens of overcrowded and injured fish in fisheries (El-Sharouny & Badran 1995) that may potentially carry pathogenic strains of water molds to naïve amphibian populations (Kiesecker et al 2001b).…”