Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis

Abstract

Sperm competition leads to increased sperm production in many taxa. This response may result from increases in testes size, changes in testicular architecture or changes in the kinetics of spermatogenesis, but the impact of each one of these processes on sperm production has not been studied in an integrated manner. Furthermore, such response may be limited in species with low mass-specific metabolic rate (MSMR), i.e., large-bodied species, because they cannot process energy and resources efficiently enough both at the organismic and cellular levels. Here we compare 99 mammalian species and show that higher levels of sperm competition correlated with a) higher proportions of seminiferous tubules, b) shorter seminiferous epithelium cycle lengths (SECL) which reduce the time required to produce sperm, and c) higher efficiencies of Sertoli cells (involved in sperm maturation). These responses to sperm competition, in turn, result in higher daily sperm production, more sperm stored in the epididymides, and more sperm in the ejaculate. However, the two processes that require processing resources at faster rates (SECL and efficiency of Sertoli cells) only respond to sperm competition in species with high MSMR. Thus, increases in sperm production with intense sperm competition occur via a complex network of mechanisms, but some are constrained by MSMR.

Figure 1. Schematic representation of the relationships between sperm competition, mass-specific metabolic rate, testicular architecture, kinetics of spermatogenesis, sperm production and numbers in sperm reserves in eutherian mammals.

a, Static 1% variations: numbers next to arrows are the relative variation in the dependent variable caused by a variation of 1% of the sample range in the independent variable. For example, there is a -0.77% decrease in SECL when we increase SC by 1%. b, c, Dynamic variations: numbers next to arrows between level 1 and level 2 variables are the relative variation in the dependent variable caused by a variation of 1% of the sample range in the independent variable (thus these values are the same as in panel a); numbers next to arrows between level 2 and level 3 variables are the relative variation in the dependent variable (level 3) caused by the change in the independent variable (level 2) due to a 1% increment in level 1. All relative variations are presented as percentages of the sample range. Relative variation percentages were calculated using the slopes and intercepts estimated by PGLS models. Arrow widths are proportional to indicated magnitudes. Abbreviations: SC: sperm competition (relative testes size); MSMR: mass-specific metabolic rate; SECL: seminiferous epithelium cycle length; ESC: efficiency of Sertoli cells; % Tub: percentage of the testicular tissue occupied by seminiferous tubules; DSP: daily sperm production; Sperm Reserves: number of spermatozoa in the caudae epididymides.