Socially-mediated compensatory growth carries hidden sperm costs in male guppies

Abstract

Phenotypic plasticity allows organisms to mitigate early-life adversity through compensatory growth, yet the long-term costs of such "catch-up" trajectories remain poorly understood, particularly when driven by social factors. While most research focuses on nutritionally induced compensation, we investigate how early social competition--independent of resource availability--shapes adult life-history trade-offs in the guppy (Poecilia reticulata). Our results show that scramble competition among peers during early development triggers compensatory growth once social constraints are removed. Crucially, we reveal a hidden reproductive cost: males exhibiting higher compensatory growth reach a similar adult size but produce significantly fewer sperm at maturity. This deficit persists even when controlling for adult body size, indicating a direct trade-off between somatic recovery and ejaculate investment. Furthermore, we find a negative association between gonopodium length and sperm count, suggesting competing allocations between pre- and postcopulatory traits during growth. These findings reveal a cryptic cost of compensatory growth, where adult morphology conceals underlying differences in reproductive quality. By demonstrating that social environments alone can recalibrate life-history trajectories, we highlight the "ghosts of competition past" as critical determinants of fitness. Our study underscores the necessity of considering ontogenetic history to fully understand the evolution of sexually selected traits in social vertebrates.