Experimental parasite infection reveals costs and benefits of paternal effects.

Joshka Kaufmann,Manfred Milinski,Tobias L Lenz,Christophe Eizaguirre,Dustin Marshall

doi:10.1111/ele.12344

Abstract

Forces shaping an individual's phenotype are complex and include transgenerational effects. Despite low investment into reproduction, a father's environment and phenotype can shape its offspring's phenotype. Whether and when such paternal effects are adaptive, however, remains elusive. Using three-spined sticklebacks in controlled infection experiments, we show that sperm deficiencies in exposed males compared to their unexposed brothers functionally translated into reduced reproductive success in sperm competition trials. In non-competitive fertilisations, offspring of exposed males suffered significant costs of reduced hatching success and survival but they reached a higher body condition than their counterparts from unexposed fathers after experimental infection. Interestingly, those benefits of paternal infection did not result from increased resistance but from increased tolerance to the parasite. Altogether, these results demonstrate that parasite resistance and tolerance are shaped by processes involving both genetic and non-genetic inheritance and suggest a context-dependent adaptive value of paternal effects.

Highlights

Understanding non-Mendelian modes of inheritance, such as parental effects, has become an important theme in evolutionary biology (Bonduriansky 2012; Rando 2012)
As exposed G2 fish encompassed both infected and uninfected individuals in approximately equal proportions, we focused on the variation in G2 body condition in response to G1 paternal effects between exposed-infected and Offspring body condition
We found a significant interaction between paternal G1 treatment and G2 infection status on G2 body condition (F1,282 = 4.14, P = 0.043; Table 1, grey shades in Fig. 3): G2 fish sired by unexposed males suffered significantly from the cost of parasite infection (Tukey post hoc test, Z = 2.58, P = 0.048), whereas G2 fish sired by exposed males did not (Tukey post hoc test, Z = À0.25, P = 0.995)

Summary

Introduction

Understanding non-Mendelian modes of inheritance, such as parental effects, has become an important theme in evolutionary biology (Bonduriansky 2012; Rando 2012). While increasingly acknowledged as an important factor, there is still controversy over the general adaptive value of parental effects (Marshall & Uller 2007). The adaptive value of a parental effect is expected to depend on the distribution of costs and benefits across parental and offspring generations and more importantly depends on the ecological context (Mousseau & Fox 1998; Marshall 2008). Studying paternal effects practically facilitates the experimental testing of adaptive non-genetic transmission, because, in contrast to the mother (e.g. through placenta, egg yolk, milk), the physiological links between father and offspring are generally very limited and can be more controlled (Curley et al 2011; Rando 2012)

Methods

Results

Conclusion