SUMMARY Self-fertile hermaphrodites have evolved independently several times in the genus Caenorhabditis [1, 2]. These XX hermaphrodites make smaller sperm than males [3, 4], which they use to fertilize their own oocytes. Since larger sperm outcompete smaller sperm in nematodes [3–5], it had been assumed that this dimorphism evolved in response to sperm competition. However, we show that it was instead caused by a developmental bias. When we transformed females of the species C. remanei into hermaphrodites [6], their sperm were significantly smaller than those of males. Because this species never makes hermaphrodites in the wild, this dimorphism cannot be due to selection. Instead, analyses of the related nematode C. elegans suggest that this dimorphism might reflect the development of sperm within the distinct physiological environment of the hermaphrodite gonad. These results reveal a new mechanism for some types of developmental bias — the effects of a novel physical location alter the development of ectopic cells in predictable ways.

Although much is known about female reproductive aging, fairly little is known about the causes of male reproductive senescence. We developed a method that facilitates culture maintenance of Caenorhabditis elegans adult males, which enabled us to measure male fertility as populations age, without profound loss of males from the growth plate. We find that the ability of males to sire progeny declines rapidly in the first half of adult lifespan and we examined potential factors that contribute towards reproductive success, including physical vigor, sperm quality, mating apparatus morphology, and mating ability. Of these, we find little evidence of general physical decline in males or changes in sperm number, morphology, or capacity for activation, at time points when reproductive senescence is markedly evident. Rather, it is the loss of efficient mating ability that correlates most strongly with reproductive senescence. Low insulin signaling can extend male ability to sire progeny later in life, although insulin impact on individual facets of mating behavior is complex. Overall, we suggest that combined modest deficits, predominantly affecting the complex mating behavior rather than sperm quality, sum up to block effective C. elegans male reproduction in middle adult life.