Sex‐dependent effects of infection on guppy reproductive fitness and offspring parasite resistance

Infection imposes energetic costs on hosts. Hosts typically respond by shifting resources, potentially affecting the quantity and quality of offspring they produce. As the sexes differ in their optimal reproductive strategies, the infection of mothers versus fathers may affect offspring quantity and quality in different ways. Here, we test how experimental infection of guppies Poecilia reticulata with the ectoparasite Gyrodactylus turnbulli affects parental reproductive fitness and offspring parasite resistance. We compared breeding pairs in which one or neither parent had previously been infected. In terms of reproductive fitness, pairs in which fathers had been infected produced more offspring than those in which mothers had been infected. Additionally, fathers who experienced the heaviest infections produced offspring ~55 days sooner than average. This result may represent terminal investment by males, especially those most affected by infection, or that males invest in reproduction at the expense of parasite defence. We found that offspring age, parental infection experience, and parental infection severity together strongly predicted offspring parasite resistance. Only among pairs in which one parent had been infected did older offspring, which were those born soonest after the parent's infection, tend to experience heavier infections. This result may reflect temporary infection-induced reductions in parental investment in offspring quality. Beyond this effect of offspring age, offspring of infected mothers experienced 105 fewer worm days than those of infected fathers: fathers, but not mothers, who experienced heavy infections themselves produced offspring that also experienced heavy infections. The parent-offspring regression for infected fathers is consistent with previous evidence that parasite resistance is heritable in this system and yields a narrow sense heritability estimate of 0.62 ± 0.12. By contrast, the mother-offspring regression (slope: -0.12 ± 0.14) provides novel insight that mothers may engage in transgenerational immune priming. Our results suggest that the sexes strike a different balance between offspring quantity and quality when faced with infection, with potentially broad implications for disease and host-parasite co-evolutionary dynamics in nature.