Natural limits on male mating sustain costly female choice, exaggerated displays, and genetic variation

Abstract

The persistence of costly female preferences, exaggerated male sexual displays, and the genetic variation underlying those displays remains a central puzzle in evolutionary biology. Classical Fisherian models explain preference-driven display exaggeration but not how costly preference and display can persist without runaway or collapse. These models assume that preferred males remain available regardless of previous mating success, precluding feedback through declining availability. Here I use a gene-centered analysis to show that allelic realized relatedness governs the indirect benefits of choice and that unlimited availability allows relatedness to remain high until genetic variation is lost. Individual-based simulations relaxing this idealization exposed negative feedback: as preference spread and concentrated mating success, preferred males reached capacity and became unavailable. Choosy females became less able to steer indirect fitness benefits toward additional copies of the preference allele, reducing allelic realized relatedness and constraining further evolution of preference and display. This transformed Fisherian runaway into stable exaggeration, allowing costly preference and display to persist for tens of thousands of generations across broad ranges of preference strength, mating capacity, and recombination rate. With autosomal display and a 1% viability cost of preference, stable exaggeration reached 16.5 additive-genetic standard deviations above matched no-preference baselines. Negative feedback generated disruptive selection on display, amplifying additive genetic variation beyond mutation-selection balance by as much as 32-fold, providing a resolution to the lek paradox--the persistence of display variation despite strong sexual selection--without invoking biased mutation or condition dependence. Z linkage of display loci, relevant to birds and other taxa with ZW sex determination, expanded the conditions supporting persistent preference and display, increased exaggeration, and further amplified genetic variation. Once inherent biological limits on male mating success are recognized, Fisherian sexual selection is revealed as a self-regulating form of gene-level cooperation.