Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus)

When females mate multiply, the competition among males for fertilizations occurs cryptically within the reproductive tract of the female. Under such sperm competition, the amount of spermatogenic tissue, the efficiency of sperm production and the capacity for sperm storage should all be under strong selection. Males of several species of fairy-wrens (Malurus) have been found to store large numbers of sperm for ejaculation, a suggested adaptation to male-biased sex ratios and high levels of reproductive promiscuity. In this study we examined the histology of testes of three species of fairy-wren: the splendid, Malurus splendens melanotus, variegated, M. lamberti assimilis, and white-winged fairy-wren, M. leucopterus leuconotus, as well as the quantity and quality (viability) of sperm in captive male splendid fairy-wrens to estimate the temporal pattern of sperm production and depletion. The daily rates of sperm production in all three species were high: 306×106 sperm/day for splendid, 125×106 sperm/day for variegated and 204×106 sperm/day for white-winged fairywrens, and the efficiency of sperm production (sperm per day per g of body mass) was several orders of magnitude greater than values reported for other domestic and wild species. For splendid fairy-wrens, the estimates of sperm production varied with the method used for estimation (range of estimates 306×106-1367×106 sperm/day). Splendid fairy-wren males held in captivity replenished their sperm reserves within 12 h, which is faster than that reported for most other species thus far. There was a negative correlation between length of sampling interval and the proportion of live sperm in ejaculate samples, indicating that males that copulate more frequently have higher-quality ejaculates. Together, both experimental and morphological estimates suggest that all three species of fairy-wren invest considerable energy in the production as well as the storage of massive numbers of sperm. Intra- and interspecific variation in the rates of sperm production is most likely linked to differences in the operational sex ratios of social groups and the opportunity for extragroup parentage.