Cryptic Forcible Insemination

Male Snakes Exploit Female Physiology, Anatomy, and Behavior to Obtain Coercive Matings

Richard Shine, Tracy Lee Langkilde, Robert T. Mason

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Whether males can inseminate uncooperative females is a central determinant of mating system evolution that profoundly affects the interpretation of phenomena such as multiple mating by females, mate choice, reproductive seasonality, and courtship tactics. Forcible insemination is usually inferred from direct physical battles between the sexes and has been dismissed on intuitive grounds for many kinds of animals. For example, snakes have elongate flexible bodies (making it difficult for a male to restrain a female physically), males are typically smaller than females, and copulation requires female cloacal gaping to enable intromission. Male garter snakes (Thamnophis sirtalis) do not display any overt aggression during courtship and simply lie over the female and exhibit rhythmic pulsating caudocephalic waves of muscular contraction; previous studies have interpreted this behavior as a mechanism for eliciting female receptivity. In contrast, we show that male garter snakes forcibly inseminate females. They do so by taking advantage of specific features of snake physiology, respiratory anatomy, and antipredator behavior. The snake lung extends along most of the body, with the large posterior section (the saccular lung) lacking any respiratory exchange surface. Rhythmic caudocephalic waves by courting male garter snakes push anoxic air from the saccular lung forward and across the respiratory surfaces such that females cannot obtain oxygen. Their stress response involves cloacal gaping, which functions in other contexts to repel predators by extruding feces and musk but in this situation permits male intromission. Thus, superficially benign courtship behaviors may involve cryptic coercion even in species for which intuition dismisses any possibility of forcible insemination.

Original languageEnglish (US)
Pages (from-to)653-667
Number of pages15
JournalAmerican Naturalist
Volume162
Issue number5
DOIs
StatePublished - Nov 1 2003

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snake
anatomy
insemination
snakes
physiology
Thamnophis
courtship
lungs
respiratory physiology
multiple mating
mate choice
copulation
aggression
mating behavior
mating systems
feces
reproductive strategy
contraction
seasonality
stress response

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics

Cite this

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title = "Cryptic Forcible Insemination: Male Snakes Exploit Female Physiology, Anatomy, and Behavior to Obtain Coercive Matings",
abstract = "Whether males can inseminate uncooperative females is a central determinant of mating system evolution that profoundly affects the interpretation of phenomena such as multiple mating by females, mate choice, reproductive seasonality, and courtship tactics. Forcible insemination is usually inferred from direct physical battles between the sexes and has been dismissed on intuitive grounds for many kinds of animals. For example, snakes have elongate flexible bodies (making it difficult for a male to restrain a female physically), males are typically smaller than females, and copulation requires female cloacal gaping to enable intromission. Male garter snakes (Thamnophis sirtalis) do not display any overt aggression during courtship and simply lie over the female and exhibit rhythmic pulsating caudocephalic waves of muscular contraction; previous studies have interpreted this behavior as a mechanism for eliciting female receptivity. In contrast, we show that male garter snakes forcibly inseminate females. They do so by taking advantage of specific features of snake physiology, respiratory anatomy, and antipredator behavior. The snake lung extends along most of the body, with the large posterior section (the saccular lung) lacking any respiratory exchange surface. Rhythmic caudocephalic waves by courting male garter snakes push anoxic air from the saccular lung forward and across the respiratory surfaces such that females cannot obtain oxygen. Their stress response involves cloacal gaping, which functions in other contexts to repel predators by extruding feces and musk but in this situation permits male intromission. Thus, superficially benign courtship behaviors may involve cryptic coercion even in species for which intuition dismisses any possibility of forcible insemination.",
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Cryptic Forcible Insemination : Male Snakes Exploit Female Physiology, Anatomy, and Behavior to Obtain Coercive Matings. / Shine, Richard; Langkilde, Tracy Lee; Mason, Robert T.

In: American Naturalist, Vol. 162, No. 5, 01.11.2003, p. 653-667.

Research output: Contribution to journalArticle

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