Dramatic fertility decline in aging C. elegans males is associated with mating execution deficits rather than diminished sperm quality

• Published in: Experimental gerontology Vol. 48; no. 11; pp. 1156 - 1166
• Main Authors: Chatterjee, Indrani, Ibanez-Ventoso, Carolina, Vijay, Priyanka, Singaravelu, Gunasekaran, Baldi, Christopher, Bair, Julianna, Ng, Susan, Smolyanskaya, Alexandra, Driscoll, Monica, Singson, Andrew
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 01-11-2013
• Subjects: Aging; Aging - pathology; Aging - physiology; Animals; C. elegans; Caenorhabditis elegans - anatomy & histology; Caenorhabditis elegans - genetics; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - physiology; Culture Media; Female; Fertility; Fertility - physiology; Forkhead Transcription Factors; Garlic; Genes, Helminth; Insulin - physiology; Male; Males; Models, Animal; Mutation; Receptor, Insulin - genetics; Receptor, Insulin - physiology; Sexual Behavior, Animal - physiology; Signal Transduction; Sperm; Sperm Count; Spermatozoa - physiology; Transcription Factors - genetics; Transcription Factors - physiology; Aging; C. elegans; Males; Sperm; Fertility
• ISSN: 0531-5565; 1873-6815
• DOI: 10.1016/j.exger.2013.07.014

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.
•New method for aging C. elegans males•Male reproductive span is only about a third of lifespan.•Short male reproductive span is not due to diminished sperm quality or vigor.•Reproductive decline correlates most strongly with loss of efficient mating ability.•Reproductive decline can be impacted by insulin signaling.