The Evolution of Parental Care in the Context of Sexual Selection: A Critical Reassessment of Parental Investment Theory

Abstract

Males and females are often defined by differences in their energetic investment in gametes. In most sexual species, females produce few large ova, whereas males produce many tiny sperm. This difference in initial parental investment is presumed to exert a fundamental influence on sex differences in mating and parental behavior, resulting in a taxonomic bias toward parental care in females and away from parental care in males. In this article, we reexamine the logic of this argument as well as the evolutionarily stable strategy (ESS) theory often used to substantiate it. We show that the classic ESS model, which contrasts parental care with offspring desertion, violates the necessary relationship between mean male and female fitness. When the constraint of equal male and female mean fitness is correctly incorporated into the ESS model, its results are congruent with those of evolutionary genetic theory for the evolution of genes with direct and indirect effects. Male parental care evolves whenever half the magnitude of the indirect effect of paternal care on offspring viability exceeds the direct effect of additional mating success gained by desertion. When the converse is true, desertion invades and spreads. In the absence of a genetic correlation between the sexes, the evolution of paternal care is independent of maternal care. Theories based on sex differences in gametic investment make no such specific predictions. We discuss whether inferences about the evolution of sex differences in parental care can hold if the ESS theory on which they are based contains internal contradictions.

Social Polyandry, Parental Investment, Sexual Selection, and Evolution of Reduced Female Gamete Size

“…The theory was founded largely on observations of animals in which males are the most competitive sex. As exceptions test the rule, species with reversed sex roles therefore offer unique opportunities for testing whether the theory is correct in that parental investment controls sexual selection (Williams 1966(Williams , 1975Trivers 1972;Berglund et al 1989;Clutton-Brock and Parker 1992;Andersson 1994;Parker and Simmons 1996;Queller 1997;Okuda 1999;Ahnesjö et al 2001;Kokko and Monaghan 2001;Wade and Shuster 2002;Berglund and Rosenqvist 2003;Wilson et al 2003). The present results suggest that causation can work both ways, that is, with sexual selection also influencing initial parental investment in form of gamete size, the basic defining trait of males and females.…”

A new record of amphisexual care in an insect with exclusive paternal care: Rhynocoris tristis (Heteroptera: Reduviidae)

“…Models describing the origins of parental care (BalshineEarn and Earn 1997; Manica and Johnstone 2004;Maynard Smith 1977;Wade and Shuster 2002) propose three resolutions to the evolutionary conflict over which parent provides care: neither parent cares; both parents care, or one parent compensates for lack of care by the other. The third option, uniparental care, can be provided exclusively by either the mother or the father, but the costs associated with care usually favor maternal over paternal care (Queller 1997).…”

Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort

“…The potential benefit of increasing mating effort at the expense of parental effort is often great, as total reproductive success tends to increase with mating success in males (Trivers 1972;Arnold 1994;Queller 1997;Wade and Shuster 2002;Shuster and Wade 2003). However, males must compete among themselves for a limited number of mating opportunities, and one male's mating success necessarily comes at the expense of another male.…”