Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird

Abstract

Duration of developmental stages in animals evolves under contrasting selection pressures of age-specific mortality and growth requirements. When relative importance of these effects varies across environments, evolution of developmental periods is expected to be slow. In birds, maternal effects on egg-laying order and offspring growth, two proximate determinants of nestling period, should enable rapid adjustment of developmental periods to even widely fluctuating mortality rates. We test this hypothesis in a population of house finches (Carpodacus mexicanus) breeding under two contrasting mortality risks: (i) a nest mite-free condition when selection on offspring survival favors a longer time in the nest; and (ii) a mite infestation when selection favors a shorter nest tenure. Mites affected survival of sons more than daughters, and females breeding under mite infestation laid male eggs last and female eggs first in the clutch, thereby reducing sons' exposure to mites and associated mortality. Strong sex bias in laying order and growth patterns enabled mite-infested offspring to achieve similar fledging size, despite a shorter nest tenure, compared with mite-free conditions. In mite-infested nests, male nestlings hatched at larger sizes, completed growth earlier, and had faster initial growth compared with mite-free nests, whereas mite-infested females grew more slowly but for a longer period of time. A combination of heavily sex-biased laying order and sex differences in growth patterns lowered mite-induced mortality by >10% in both sexes. Thus, strong maternal effects can account for frequently observed, but theoretically unexpected, concordance of mortality risks and growth patterns, especially under fluctuating ecological conditions.