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, 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,
parental infection experience did not affect the size, body condition, or
number of offspring produced, but fathers who experienced the heaviest
infections produced offspring ~55 days sooner than average. This result
may represent terminal investment by the males most affected by infection,
or may indicate that these males have a faster pace of life, investing 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, older offspring, which were
those born soonest after the parent’s infection, tended to experience
heavier infections. This result may therefore 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, that experienced heavy infections themselves produced
offspring that also experienced heavy infections. The parent-offspring
regression for infected fathers is therefore consistent with previous
evidence that parasite resistance is heritable in this system, and yields
a narrow sense heritability estimate of 0.69±0.13. By contrast, the
mother-offspring regression (slope: -0.13±0.17) provides novel insight
that mothers may engage in transgenerational immune priming. Overall, 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 coevolutionary dynamics
in nature.