Rapid adaptation to mammalian sociality via sexually selected traits

Abstract

BackgroundLaboratory studies show that the components of sexual selection (e.g., mate choice and intrasexual competition) can profoundly affect the development and fitness of offspring. Less is known, however, about the total effects of sexual selection on offspring in normal social conditions. Complex social networks, such as dominance hierarchies, regulate the opportunity for mating success, and are often missing from laboratory studies. Social selection is an extended view of sexual selection that incorporates competition during sexual and nonsexual interactions, and predicts complex evolutionary dynamics. Whether social selection improves or constrains offspring fitness is controversial.ResultsTo identify fitness consequences of social selection, wild-derived mice that had bred under laboratory conditions for eight generations were re-introduced to naturalistic competition in enclosures for three consecutive generations (promiscuous line). In parallel, a control lineage bred in cages under random mate assignment (monogamous line). A direct competition experiment using second-generation animals revealed that promiscuous line males had greater reproductive success than monogamous line males (particularly during extra-territorial matings), in spite of higher mortality and equivalent success in social dominance and sperm competition. There were no major female fitness effects (though promiscuous line females had fewer litters than monogamous line females). This result suggested that selection primarily acted upon a sexually attractive male phenotype in the promiscuous line, a hypothesis we confirmed in female odor and mating preference trials.ConclusionsWe present novel evidence for the strength of sexual selection under normal social conditions, and show rapid male adaptation driven largely by sexual trait expression, with tradeoffs in survivorship and female fecundity. Re-introducing wild-derived mice to competition quickly uncovers sexually selected phenotypes otherwise lost in normal colony breeding.

Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression

“…E-mail: adamnelson@fas.harvard.edu. revealed female mating and odor preferences for promiscuousline males (14). These results suggested that returning mice to sociality favored an attractive male-specific phenotype characterized by enhanced pheromone signaling, but conspicuously lacking in vigor and viability, a result consistent with the sexy sons hypothesis of sexual selection (14).…”

“…Adult "parents" experienced one of two treatments for roughly 8 wk: competition (C) or noncompetition (NC). Using the same protocol to generate promiscuousline and monogamous-line mice (14), C males and females were introduced to enclosures where they competed for resources, mates, and social dominance (12,14) whereas NC males and females experienced 8 wk in monogamous breeding cages. Following a brief intermission period (during which pups from pregnant females were removed), females and males were assigned, respectively, to monogamous breeding in the following four-way reciprocal breeding design: C × C; C × NC; NC × C; and NC × NC.…”

“…To address this question, we measured female attraction to artificial scent marks that were identical except for MUP concentration. Using the same preference arena used to identify female attraction to promiscuous-line males (14), one female per trial was given a choice between high concentration (20 mg/mL) vs. low concentration (3 mg/mL) urine spots derived from a single male, thereby controlling for potential preferences based on the identity of the male (Fig. 5A).…”

“…Thus, before testing, neither promiscuous-line nor monogamous-line individuals experienced seminatural conditions. A direct competition experiment in enclosures revealed fitness effects on males, but not females: compared with monogamous-line males, promiscuous-line males sired significantly more offspring and were favored by females during extraterritorial mating (14). Strikingly, promiscuous-line males had reduced survivorship and equivalent success in territory defense.…”

Sexual selection constrains the body mass of male but not female mice

“…Within these enclosures some, but not all, pressures of natural selection (e.g., predation) are absent, and most sexual selection pressures are present (including male–male competition and female choice ((Meagher, Penn, & Potts, 2000; Nelson, Colson, Harmon, & Potts, 2013))). Therefore, by assessing the reproductive success of mice in semi‐natural enclosures, one can evaluate a trait's influence on fitness in the context of moderate levels of natural selection and high levels of sexual selection.…”