Skip to main content
Log in

Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis

  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Summary

Many adaptations have arisen in response to spern competition. In garter snakes, males produce copulatory plugs that are thought to prevent such competition. We tested this assumption using paternity exclusion techniques with electrophoretic data from 32 litters of snakes collected from two populations. Multiple paternity was confirmed in 50% of the litters examined (13/22 Michigan litters; 3/10 Wisconsin litters), and we estimate that as many as 72% of the litters may have been multiply sired. The presence of multiple paternity was also confirmed using the technique of genotypic regression. Mean relatedness in litters with evidence of multiple paternity was 0.390±0.053; in litters lacking such evidence mean relatedness was 0.498±0.022. Thus our data reveal a high incidence of multiple paternity in these snakes and suggest that their adaptations to prevent sperm competition are surprisingly ineffective.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akin E, Levene H, Levine L, Rockwell R (1984) A conservative procedure for the estimation of multiple insemination in Drosophila. Am Nat 124:723–737

    Google Scholar 

  • Aleksiuk M, Gregory P (1974) Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 1974:681–689

    Google Scholar 

  • Arnold SJ (1981a) Behavioral variation in natural populations. I. Phenotypic, genetic and environmental correlations between chemoreceptive responses to prey in the garter snake, Thamnophis elegans. Evolution 35:489–509

    Google Scholar 

  • Arnold SJ (1981b) The microevolution of feeding behavior. In: Kamil AC, Sargent TD (eds) Foraging behavior: ecological, ethological, and psychological approaches. Garland Publ Inc, New York, pp 409–453

    Google Scholar 

  • Arnold SJ (1988) Quantitative genetics and selection in natural populations: Microevolution of vertebral numbers in the garter snake Thamnophis elegans. In: Weir BS, Eisen EJ, Goodman MM, Namkoong G (eds) Proceedings of the second international conference on quantitative genetics. Sinauer Assoc Inc, Sunderland, Massachusetts, pp 619–636

    Google Scholar 

  • Arnold SJ, Bennett AF (1984) Behavioral variation in natural populations. III. Antipredator displays in the garter snake Thamnophis radix. Anim Behav 32:1108–1118

    Google Scholar 

  • Avise JC, Shapiro DY (1986) Evaluating kinship of newly settled juveniles within social groups of the coral reef fish Anthias squamipinnis. Evolution 40:1051–1059

    Google Scholar 

  • Ayres FA, Arnold SJ (1983) Behavioral variation in natural populations. IV. Mendelian models and heritability of a feeding response in the garter snake, Thamnophis elegans. Heredity 51:405–413

    Google Scholar 

  • Blanchard FC (1943) A test of fecundity of the garter snake Thamnophis sirtalis sirtalis (Linnaeus) in the year following the year of insemination. Pap Mich Acad Sci Arts Lett 28(1942):313–317

    Google Scholar 

  • Blanchard FN, Blanchard FC (1941) The inheritance of melanism in the garter snake Thamnophis sirtalis sirtalis (Linnaeus), and some evidence of effective autumn mating. Pap Mich Acad Sci Arts Lett 26(1940):177–193

    Google Scholar 

  • Blanchard FN, Blanchard FC (1942) Mating of the garter snake Thamnophis sirtalis sirtalis (Linnaeus). Pap Mich Acad Sci Arts Lett 27(1941):215–234

    Google Scholar 

  • Devine MC (1975) Copulatory plugs in snakes: enforced chastity. Science 187:844–845

    Google Scholar 

  • Devine MC (1977) Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes. Nature 267:345–346

    Google Scholar 

  • Devine MC (1984) Potential for sperm competition in reptiles: behavioral and physiological consequences. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press Inc, Orlando, pp 509–521

    Google Scholar 

  • Fitch HS (1965) An ecological study of the garter snake, Thamnophis sirtalis. Univ Kansas Mus Nat Hist Publ 15(10):493–564

    Google Scholar 

  • Fox W (1956) Seminal receptacles of snakes. Anat Rec 124:519–540

    Google Scholar 

  • Garland T (1988) Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42:335–350

    Google Scholar 

  • Garstka WR, Crews D (1985) Mate preference in garter snakes. Herpetologica 41:9–19

    Google Scholar 

  • Garstka WR, Camazine B, Crews D (1982) Interactions of behavior and physiology during the annual reproductive cycle of the red-sided garter snake (Thamnophis sirtalis parietalis). Herpetologica 38:104–123

    Google Scholar 

  • Garstka WR, Tokarz RR, Diamond M, Halpert A, Crews D (1985) Behavioral and physiological control of yolk synthesis and deposition in the female red-sided garter snake (Thamnophis sirtalis parietalis). Horm Behav 19:137–153

    Google Scholar 

  • Gibson AR, Falls JB (1975) Evidence for multiple insemination in the common garter snake Thamnophis sirtalis. Can J Zool 53:1362–1368

    Google Scholar 

  • Gregory PT (1974) Patterns of spring emergence of the red-sided garter snake (Thamnophis sirtalis parietalis) in the Interlake region of Manitoba. Can J Zool 52:1063–1069

    Google Scholar 

  • Gregory PT (1976) Life history parameters of the red-sided garter snake (Thamnophis sirtalis parietalis) in an extreme environment, the Interlake region of Manitoba. Natl Mus Nat Sci Ottawa Publ Zool No 13

  • Halliday T (1980) Sexual strategy. Univ of Chicago Press, Chicago

    Google Scholar 

  • Halliday T, Arnold SJ (1987) Multiple mating by females: per-spective from quantitative genetics. Anim Behav 35:939–940

    Google Scholar 

  • Halpert AP, Garstka WR, Crews D (1982) Sperm transport and storage and its relation to the annual sexual cycle of the female red-sided garter snake, Thamnophis sirtalis parietalis. J Morphol 174:149–159

    Google Scholar 

  • Harris H, Hopkinson DA (1978) Handbook of enzyme electrophoresis in human genetics. Elsevier, New York

    Google Scholar 

  • Joy JE, Crews D (1985) Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis). J Comp Psychol 99:145–149

    Google Scholar 

  • Lefevre G, Jonsson UB (1962) Sperm transfer, storage, displacement and utilization in Drosophila melanogaster. Genetics 47:1719–1736

    Google Scholar 

  • Levine L, Akin E, Olvera O, Gaso MI, Rockwell RF, Gonzalez F, de la Rosa ME, Guzman J (1987) Chromosomal and behavioral studies of Mexican Drosophila. V. Frequencies of multiple insemination in three natural populations. Am Nat 129:458–462

    Google Scholar 

  • Martan J, Shepherd BA (1976) The role of the copulatory plug in reproduction of the guinea pig. J Exp Zool 196:79–84

    Google Scholar 

  • Pamilo P (1984) Genotypic correlation and regression in social groups: multiple alleles, multiple loci and subdivided populations. Genetics 107:307–320

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Google Scholar 

  • Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press Inc, Orlando, pp 1–60

    Google Scholar 

  • Parker GA, Smith JL (1975) Sperm competition and the evolution of the precopulatory passive phase behaviour in Locusta migratoria migratorioides. J Entomol (A) 49:155–171

    Google Scholar 

  • Rahn H (1940) Sperm viability in the uterus of the garter snake, Thamnophis. Copeia 1940:109–115

    Google Scholar 

  • Ross P, Crews D (1977) Influence of the seminal plug on mating behaviour in the garter snake. Nature 267:344–345

    Google Scholar 

  • Ross P, Crews D (1978) Stimuli influencing mating behavior in the garter snake, Thamnophis radix. Behav Ecol Sociobiol 4:133–142

    Google Scholar 

  • Schuett GW, Gillingham JC (1986) Sperm storage and multiple paternity in the copperhead, Agkistrodon contortrix. Copeia 1986:807–811

    Google Scholar 

  • Schwartz JM (1989) Multiple paternity and offspring variability in wild populations of the garter snake Thamnophis sirtalis (Colubridae). Unpublished PhD dissertation, University of Tennessee, Knoxville, Tennessee, USA

  • Selander RK, Smith MH, Yang SY, Johnson WE, Gentry JB (1971) Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Studies in Genetics VI. Univ Texas Publ 7103:49–90

    Google Scholar 

  • Sivinski J (1984) Sperm in competition. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press Inc, Orlando, pp 85–115

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Sec. Ed. Freeman, San Francisco

    Google Scholar 

  • Stewart GR (1972) An unusual record of sperm storage in a female garter snake (genus Thamnophis). Herpetologica 28:346–347

    Google Scholar 

  • Still B, Madsen T, Niklasson M (1986) Multiple paternity in the adder, Vipera berus. Oikos 47:173–175

    Google Scholar 

  • Waage JK (1984) Sperm competition and the evolution of odonate mating systems. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press Inc, Orlando, pp 251–290

    Google Scholar 

  • Whittier JM, Crews D (1986) Ovarian development in red-sided garter snakes, Thamnophis sirtalis parietalis: relationship to mating. Gen Comp Endocrino 61:5–12

    Google Scholar 

  • Whittier JM, Mason RT, Crews D (1985) Mating in the red-sided garter snake, Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior. Behav Ecol Sociobiol 16:257–261

    Google Scholar 

  • Zweifel RG, Dessauer HC (1983) Multiple insemination demonstrated experimentally in the kingsnake, Lampropeltis getulus. Experientia 39:317–319

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwartz, J.M., McCracken, G.F. & Burghardt, G.M. Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis . Behav Ecol Sociobiol 25, 269–273 (1989). https://doi.org/10.1007/BF00300053

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00300053

Keywords

Navigation