Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited

Abstract

During the spring emergence of red‐sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba, Canada, the operational sex ratio is strongly skewed towards males, who scramble to locate and court newly emerged females. A high frequency of multiple paternity litters suggests that the females are promiscuous; the gelatinous copulatory plugs (CPs) deposited by males may confer fitness benefits via passive mate guarding. Because precopulatory female choice is limited in large mating aggregations, sexual conflict may place a premium on preventing females from ejecting male sperm. In snakes, sperm are produced in the testes and delivered through the ductus deferens, and the CP is thought to be produced by the renal sexual segment and conveyed through the ureter. We manipulated the delivery of the two fluids separately by surgically ligating the ducts. Ureter‐ligated males did not produce a CP, causing their sperm to leak out of the female's cloaca immediately after copulation. Contrary to previous suggestions, histology revealed sperm distributed throughout the CP. Thus, the CP may function as a spermatophore: the protein matrix contains the sperm, which are liberated gradually as the plug dissolves. The likelihood of a male depositing a CP fell significantly after his second mating, perhaps limiting his reproductive success. These results challenge the hypothesis that passive mate guarding is the primary function of the CP in T. sirtalis parietalis. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 893–907.

Size dependence in non-sperm ejaculate production is reflected in daily energy expenditure and resting metabolic rate

“…On average, larger males deposit slightly larger plugs and longer copulations tend to produce larger plugs as well. Nevertheless, there is no relationship between male size and copulation duration, indicating that larger males deposit plug material more quickly, perhaps because they have greater storage capacity and associated delivery ducts than smaller males (Friesen et al, 2013(Friesen et al, , 2014cShine et al, 2000a). Secondly, copulating males have increased blood lactate compared with courting males, which suggests that mating incurs an additional energetic cost over courtship alone (Shine et al, 2004b).…”

“…In addition to the temporal separation of mating and feeding, redsided garter snakes display another convenient characteristic for the study of the costs of seminal fluid production: they exhibit a dissociated reproductive pattern (Crews, 1984), in which spermatogenesis occurs during late summer and ceases as the testes regress in the autumn; males then store sperm over winter for use in the spring mating season (Crews, 1984;Crews et al, 1984;Krohmer et al, 1987). While the ductus deferens and testes contribute a few substances to semen in the spring, most are produced in the late summer and autumn when spermatogenesis is ongoing (Marinho et al, 2009); however, the largest non-sperm contribution to the seminal fluid is produced during the spring (Friesen et al, 2013;Krohmer, 2004a).…”

“…The predominate component of the seminal fluid of the redsided garter snake forms a large, gelatinous copulatory plug (hereafter 'plug') that is deposited within the female's vaginal pouch during copulation (Devine, 1975;Friesen et al, 2013;Shine et al, 2000a). The plug is a spermatophore that encases the sperm (sensu Mann, 1984) and thus prevents sperm leakage or ejection while also delaying females from remating, and thus is crucial for male reproductive success (Devine, 1975(Devine, , 1984Friesen et al, 2013;Shine et al, 2000a).…”

“…The plug is a spermatophore that encases the sperm (sensu Mann, 1984) and thus prevents sperm leakage or ejection while also delaying females from remating, and thus is crucial for male reproductive success (Devine, 1975(Devine, , 1984Friesen et al, 2013;Shine et al, 2000a). The plug material is produced in the kidneys (Friesen et al, 2013) within apocrine cells of the distal tubules collectively called the renal sexual segment (Aldridge et al, 2011). The apocrine cells of the renal sexual segment are sexually dimorphic and hypertrophied and actively produce plug material in males during the spring mating season (Krohmer, 2004a,b).…”

“…the plug) are replenished after mating if they are exhausted (Bishop, 1959;Krohmer, 2004b;Krohmer et al, 2004). Males are limited in the number of plugs they can deposit over a short period (1-2 plugs per day; Friesen et al, 2013;Shine et al, 2000a), but males will still copulate and not leave a plug (Friesen et al, 2013). In this system, the temporal separation of the key physiological processes that contribute to male mating success allows us to separate the cost of producing non-sperm ejaculate components and the cost of courtship from the cost of sperm production.…”