Beyond sperm competition: perspectives on sperm economy from external fertilizing fishes

Abstract

Research on sperm economy has traditionally focused on sperm competition as a major selective pressure shaping sperm production and allocation. In this review, we broaden this perspective by considering how other reproductive and ecological pressures influence the management of a costly and finite sperm supply. We synthesize evidence showing that in externally fertilizing fishes, high mating frequency, low female fecundity, prolonged spawning, rapid sperm dilution and costly male reproductive investment can favour sperm-economy strategies even when sperm competition is weak or absent. Across fish taxa, these constraints have led to convergent behavioural and physiological adaptations, including fractionated ejaculation, temporal matching of sperm release to egg deposition and manipulation of the fertilization microenvironment, which improve fertilization efficiency while minimizing sperm expenditure. We further highlight a recurring association between these strategies and semi-cystic spermatogenesis, consistent with the possibility that optimization of sperm use extends beyond ejaculate allocation to the regulation of sperm production during spermatogenesis. By integrating evidence from behaviour to reproductive physiology, this review reframes sperm economy as a general resource-allocation problem, with sperm competition representing one of several selective pressures. Externally fertilizing fishes emerge as an exceptional model for understanding the diverse evolutionary routes by which males optimize reproductive investment.