Antagonistic parent-offspring co-adaptation

Abstract

Background: In species across taxa, offspring have means to influence parental investment (PI). PI thus evolves as an interacting phenotype and indirect genetic effects may strongly affect the co-evolutionary dynamics of offspring and parental behaviors. Evolutionary theory focused on explaining how exaggerated offspring solicitation can be understood as resolution of parent-offspring conflict, but the evolutionary origin and diversification of different forms of family interactions remains unclear.

Methodology/principal findings: In contrast to previous theory that largely uses a static approach to predict how "offspring individuals" and "parental individuals" should interact given conflict over PI, we present a dynamic theoretical framework of antagonistic selection on the PI individuals obtain/take as offspring and the PI they provide as parents to maximize individual lifetime reproductive success; we analyze a deterministic and a stochastic version of this dynamic framework. We show that a zone for equivalent co-adaptation outcomes exists in which stable levels of PI can evolve and be maintained despite fast strategy transitions and ongoing co-evolutionary dynamics. Under antagonistic co-adaptation, cost-free solicitation can evolve as an adaptation to emerging preferences in parents.

Conclusions/significance: We show that antagonistic selection across the offspring and parental life-stage of individuals favors co-adapted offspring and parental behavior within a zone of equivalent outcomes. This antagonistic parent-offspring co-adaptation does not require solicitation to be costly, allows for rapid divergence and evolutionary novelty and potentially explains the origin and diversification of the observed provisioning forms in family life.

Figure 1. Transmission dynamics of provisioning genes (blue boxes) and solicitation genes (red boxes).

Filled boxes indicate the gene is expressed in that life-stage, hatched boxes that the gene in not expressed. Arrows depict the path through which genes get passed on to the next generation.

Figure 2. Fitness model used throughout.

Panel A depicts how survival S is determined by the amount of obtained parental investment (f_o,t) (for different shape parameters k), B how parental fecundity F changes with the amount of provided PI (f_p,t) (for different total resources available for reproduction; parameter m), and C how individual lifetime fitness W changes in relation to PI when f_o = f_p and for different values of k.

Figure 3. Co-adaptation equilibrium and neutral stability.

In A the fitness surface displaying the neutral curve for co-adapted associations of offspring solicitation and parental sensitivity for a fixed value of β is shown. B illustrates a typical dynamics of the system from two different sets of initial conditions (solid versus dashed lines). Red lines are for parental sensitivity α, green lines for offspring solicitation ξ and blue lines for the baseline provisioning β; clearly, under different initial conditions the system reaches different stable equilibria that are part of the stable equilibrium ‘curve’ in A.

Figure 4. Simulation outcomes with parental sensitivity fixed.

a ₁ represents an insensitive parental strategy, and a ₅ the most sensitive parental strategy. The solicitation locus is allowed to mutate among the five alleles and evolve. x ₁ is a non-soliciting strategy, x ₅ the highest solicitation strategy. and adapt to the parental sensitivity present in the parental sub-population. The mean and 95% percentiles of the distribution of evolutionary outcomes are shown for the frequencies of each solicitation allele after 500 generations.

Figure 5. Simulation outcome with offspring solicitation and parental sensitivity co-evolving.

Example of a single simulation run. Panel A) shows the evolution of the population mean level of PI (the dashed red line reflects the theoretical optimum level of PI for the chosen parameter values). B) the evolving frequencies of the five solicitation alleles, and C) the evolving frequencies of the five sensitivity alleles.

Figure 6. Time dynamics in the stochastic simulations.

The co-evolutionary time-dynamics for the level of PI, solicitation allele frequencies and sensitivity allele frequencies. Shown are the mean and 95% percentiles for the coefficients of variation (C.V.) calculated over the final 250 generations and across 100 simulation runs.