Behavioural correlates with hemipenis morphology in New World natricine snakes

Biological Journal of the Linnean Society

Volumn 98, Issue 1, 2009, Pages 110-120

  King, Richard B ^a   Jadin, Robert C ^b   Grue, Michael ^a   Walley, Harlan D ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

Author keywords

Copulation duration; Hemipenes; Nerodia; Sexual conflict; Thamnophis

Indexed keywords

BEHAVIORAL RESPONSE; BODY SIZE; COPULATION; EVOLUTIONARY BIOLOGY; MATING BEHAVIOR; ORNAMENTATION; PHENOTYPIC PLASTICITY; PHYLOGENY; SEXUAL CONFLICT; SNAKE; SPECIES OCCURRENCE;

NERODIA; SERPENTES; THAMNOPHIS; THAMNOPHIS RADIX; THAMNOPHIS SIRTALIS;

EID: 69449099656     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01270.x     Document Type: Article

References (85)

1. Alfaro ME, Arnold SJ. 2001. Molecular systematics and evolution of Regina and Thamnophiine snakes. Molecular Phylogenetics and Evolution 21 : 408 423.
2. Anderson M. 1994. Sexual selection. Princeton, NJ : Princeton University Press.
3. Arnqvist G, Rowe L. 2005. Sexual conflict. Princeton, NJ : Princeton University Press.
4. Ball RL. 1978. The courtship and mating behavior of a Mexican garter snake Thamnophis melanogaster. MS Thesis, University of Oklahoma.
5. Bernstein S, Bernstein R. 2002. Allometry of male genitalia in a species of soldier beetle: support for the one-size-fits-all hypothesis. Evolution 56 : 1707 1710.
6. Birkhead TR, Moller AP. 1998. Sperm competition and sexual selection. San Diego, CA : Academic Press.
7. Blouin-Demers G, Gibbs HL, Weatherhead PJ. 2005. Genetic evidence for sexual selection in black ratsnakes, Elaphe obsoleta. Animal Behaviour 69 : 225 234.
8. Branch WR, Wade EOZ. 1976. Hemipenial morphology of British snakes. British Journal of Herpetology 5 : 548 553.
9. Brown EE. 1940. Life history and habits of the northern water snake, Natrix sipedon sipedon Linne. PhD Thesis, Cornell University, Ithaca.
10. Böhme W. 1988. Zur Genitalmorphologie der Sauria: funktionelle und stammesgeschichtliche Aspekten. Bonner Zoologische Mongraphien 27 : 1 176.
11. Chapman T, Arnqvist G, Bangham J, Rowe L. 2003. Sexual conflict. Trends in Ecology and Evolution 18 : 41 47.
12. Darwin C. 1871. The descent of man and selection in relation to sex. London : John Murray.
13. de Queiroz A, Lawson R, Lemos-Espinal JA. 2002. Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: how much DNA sequence is enough? Molecular Phylogenetics and Evolution 22 : 315 329.
14. Devine MC. 1977. Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes. Nature 267 : 345 346.
15. Dowling HG, Duellman WE. 1978. Systematic herpetology: a synopsis of families and higher categories. New York, NY : HISS Publications.
16. Dowling HG, Savage JM. 1960. A guide to the snake hemipenis: a survey of basic structure and systematic characteristics. Zoologica 45 : 17 28.
17. Dubey S, Brown GP, Madsen T, Shine R. 2009. Sexual selection favours large body size in males of a tropical snake (Stegonotus cucullatus, Colubridae). Animal Behaviour 77 : 177 182.
18. Duvall D, Arnold SJ, Schuett GW. 1992. Pitviper mating systems: ecological potential, sexual selection, and microevolution. In : Campbell JA, Brodie ED, Jr., eds. Biology of the pitvipers. Tyler, TX : Selva, 321 336.
19. Eberhard W. 1985. Sexual selection and animal genitalia. Cambridge, MA : Harvard University Press.
20. Eberhard W, Rodriguez RL, Polihronakis M. 2009. Pitfalls in understanding the functional significance of genital allometry. Journal of Evolutionary Biology 22 : 435 445.
21. Ernst CH, Ernst EM. 2003. Snakes of the United States and Canada. Washington, DC : Smithsonian Books.
22. Fisher RA. 1930. The genetical theory of natural selection. London : Oxford University Press.
23. Fitze PS, Le Galliard J-F. 2008. Operational sex ratio, sexual conflict and the intensity of sexual selection. Ecology Letters 11 : 432 439.
24. Garner TWJ, Gregory PT, McCracken GF, Burghardt GM, Koop BF, McLain SE, Nelson RJ. 2002. Geographic variation of multiple paternity in the common garter snake (Thamnophis sirtalis). Copeia 2002 : 15 23.
25. 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. (Pubitemid 15275955)
26. Gibbons JW, Dorcas ME. 2004. North American watersnakes: a natural history. Norman, OK : University of Oklahoma Press.
27. Gillingham JC, Chambers JA. 1980. Observations on the reproductive behaviour of the eastern indigo snake, Drymarchon corais couperi, in captivity. British Journal of Herpetology 6 : 99 100.
28. Gillingham JC, Chambers JA. 1982. Courtship and pelvic spur use in the Burmese python, Python molurus bivittatus. Copeia 1982 : 193 196.
29. Gregory PT. 1977. Life-history parameters of the red-sided garter snake (Thamnophis sirtalis parietalis) in an extreme environment, the interlake region of Manitoba. National Museums of Canada Publications in Zoology 13 : 1 44.
30. Hosken DJ, Stockley P. 2004. Sexual selection and genital evolution. Trends in Ecology and Evolution 19 : 87 93.
31. Huff TA. 1980. Captive propagation of the subfamily Boinae with emphasis on the genus Epicrates. In : Murphy JB, Collins JT, eds. Reproductive biology and diseases of captive reptiles. Lawrence, KS : Society for the Study of Amphibians and Reptiles, 125 134.
32. Keogh JS. 1999. Evolutionary implications of hemipenial morphology in the terrestrial Australian elapid snakes. Zoological Journal of the Linnean Society 125 : 239 278.
33. King RB. 2003. Mendelian inheritance of melanism in the garter snake Thamnophis sirtalis. Herpetologica 59 : 486 491.
34. King RB, Milstead WB, Gibbs HL, Prosser MR, Burghardt GM, McCracken GF. 2001. Application of microsatellite DNA markers to discriminate between maternal and genetic effects on scalation and behavior in multiply-sired garter snake litters. Canadian Journal of Zoology 79 : 121 128.
35. Kissner KJ, Weatherhead PJ, Gibbs HL. 2005. Experimental assessment of ecological and phenotypic factors affecting male success and polyandry in northern watersnakes, Nerodia sipedon. Behavioral Ecology and Sociobiology 59 : 207 214.
36. Lawson R, Slowinski JB, Crother BI, Burbrink FT. 2005. Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 37 : 581 601.
37. Luiselli L. 1996. Individual success in mating balls of the grass snake, Natrix natrix: size is important. Journal of Zoology 239 : 731 740.
38. McCracken GF, Burghardt GM, Houts SE. 1999. Microsatellite markers and multiple paternity in the garter snake Thamnophis sirtalis. Molecular Ecology 8 : 1475 1480.
39. Madsen T, Shine R. 1993. Male mating success and body size in European grass snakes. Copeia 1993 : 561 564.
40. Martins EP. 1996. Phylogenies and the comparative method in animal behaviour. Oxford : Oxford University Press.
41. Mittleman MB. 1947. Miscellaneous notes on Indiana amphibians and reptiles. American Midland Naturalist 38 : 446 484.
42. Murphy JB, Barker DG. 1980. Courtship and copulation of the Ottoman viper (Vipera xanthina) with special reference to the use of the hemipenes. Herpetologica 36 : 165 170.
43. Noble GK. 1937. The sense organs involved in the courtship of Storeria, Thamnophis and other snakes. Bulletin of the American Museum of Natural History 73 : 673 725.
44. Olsson M, Madsen T. 1998. Sexual selection and sperm competition in reptiles. In : Birkhead TR, Moller AP, eds. Sperm competition and sexual selection. San Diego, CA : Academic Press, 503 577.
45. Perry-Richardson JJ, Schofield CW, Ford NB. 1990. Courtship of the garter snake, Thamnophis marcianus, with a description of a female behavior for coitus interruption. Journal of Herpetology 24 : 76 78.
46. Pfrender M, Mason RT, Wilmslow JT, Shine R. 2001. Thamnophis sirtalis parietalis (Red-sided Gartersnake). Male-male copulation. Herpetological Review 32 : 52.
47. Pinou T, Vicario S, Jarschner M, Caccone A. 2004. Relict snakes of North America and their relationships within Caenophidia, using likelihood-based Bayesian methods on mitochondrial sequences. Molecular Phylogenetics and Evolution 32 : 563 572.
48. Pisani GR. 1967. Notes on the courtship and mating behaviour of Thamnophis brachystoma (Cope). Herpetologica 23 : 112 115.
49. Pisani GR. 1976. Comments on the courtship and mating mechanics of Thamnophis (Reptilia, Serpentes, Colubridae). Journal of Herpetology 10 : 139 142.
50. Ramos M, Coddington JA, Christenson TE, Irschick DJ. 2005. Have male and female genitalia coevolved? A phylogenetic analysis of genitalic morphology and sexual size dimorphism in web-building spiders (Araneae: Araneoidea). Evolution 59 : 1989 1999.
51. Ramsey LW. 1946. Captive specimens of Tropidoclonion lineatum. Herpetologica 3 : 112.
52. Riches RJ. 1967. Early maturity in garter snakes (Thamnophis elegans elegans). British Journal of Herpetology 4 : 16 17.
53. Ross P, Crews D. 1977. Influence of the seminal plug on mating behaviour in the garter snake. Nature 267 : 344 345.
54. Ross P, Crews D. 1978. Stimuli influencing mating behavior in the garter snake, Thamnophis radix. Behavioural Ecology and Sociobiology 4 : 133 142.
55. Rossman DA, Eberle WG. 1977. Patterns of the genus Natrix, with preliminary observations on evolutionary trends in natricine snakes. Herpetologica 33 : 34 43.
56. Rossman DA, Ford NB, Seigel RA. 1996. The garter snakes: evolution and ecology. Norman, OK : University of Oklahoma Press.
57. Royle NJ, Hartley IR, Parker GA. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature 416 : 733 736.
58. Ruthven AG. 1912. On the breeding habits of Butler's garter snake. The Biological Bulletin 24 : 18 20.
59. Schleich HH, Kästle W, Kabisch K. 1996. Amphibians and reptiles of North Africa. Koenigstein : Koeltz Scientific Books.
60. Schwartz JM, McCracken GF, Burghardt GM. 1989. Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis. Behavioral Ecology and Sociobiology 25 : 269 273.
61. Secor SM. 1987. Courtship and mating behavior of the speckled kingsnake, Lampropeltis getulus holbrooki. Herpetologica 43 : 15 28.
62. Shine R, Harlow P, LeMaster MP, Moore IT, Mason RT. 2000a. The transvestite serpent: why do male garter snakes court (some) other males? Animal Behaviour 59 : 349 359.
63. Shine R, Langkilde T, Mason RT. 2003a. The opportunistic serpent: male garter snakes adjust courtship tactics to mating opportunities. Behaviour 140 : 1509 1526. (Pubitemid 38135336)
64. Shine R, Langkilde T, Mason RT. 2003b. Cryptic forcible insemination: male snakes exploit female physiology, anatomy, and behavior to obtain coercive matings. American Naturalist 162 : 653 667.
65. Shine R, Langkilde T, Mason RT. 2004a. Courtship tactics in garter snakes: how do a male's morphology and behaviour influence his mating success? Animal Behaviour 67 : 477 483.
66. Shine R, Mason RT. 2005. Does large body size in males evolve to facilitate forcible insemination? A study on garter snakes. Evolution 59 : 2426 2432.
67. Shine R, O'Conner D, LeMaster MP, Mason RT. 2001. Pick on someone your own size: ontogenetic shifts in mate choice by male garter snakes result in size-assortative mating. Animal Behaviour 61 : 113 1141.
68. Shine R, O'Connor D, Mason RT. 2000b. Sexual conflict in the snake den. Behavioral Ecology Sociobiology 48 : 392 401.
69. Shine R, Olsson MM, LeMaster MP, Moore IT, Mason RT. 2000c. Are snakes right-handed? Asymmetry in hemipenis size and usage in garter snakes (Thamnophis sirtalis). Behavioral Ecology 11 : 411 415.
70. Shine R, Olsson MM, Mason RT. 2000d. Chastity belts in gartersnakes: the functional significance of mating plugs. Biological Journal of the Linnean Society 70 : 377 390.
71. Shine R, Olsson MM, Moore IT, LeMaster MP, Green M, Mason RT. 2000e. Body size enhances mating success in male garter snakes. Animal Behaviour 59 : F4 F11.
72. Shine R, Phillips B, Langkilde T, Lutterschmidt DI, Waye H, Mason RT. 2004b. Mechanisms and consequences of sexual conflict in gartersnakes (Thamnophis sirtalis, Colubridae). Behavioral Ecology 15 : 654 660.
73. Shine R, Phillips B, Waye H, LeMaster M, Mason RT. 2003c. The lexicon of love: what cues cause size-assortative courtship by male garter snakes? Behavioral Ecology and Sociobiology 53 : 234 237.
74. Shine R, Phillips B, Waye H, LeMaster M, Mason RT. 2003d. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behavioral Ecology and Sociobiology 54 : 162 166.
75. Shine R, Wall M, Langkilde T, Mason RT. 2005. Battle of the sexes: forcibly inseminating male garter snakes target courtship to more vulnerable females. Animal Behaviour 70 : 1133 1140.
76. Stallman RR, Harcourt AH. 2006. Size matters: the (negative) allometry of copulatory duration in mammals. Biological Journal of the Linnean Society 87 : 185 193.
77. Stanford KM, King RB. 2004. Growth, survival and reproduction in a semi-urban population of the Plains garter snake, Thamnophis radix, in northern Illinois. Copeia 2004 : 465 478.
78. Taylor EH. 1942. Mexican snakes of the genera Adelophis and Storeria. Herpetologica 2 : 75 79.
79. Trapido H. 1944. The snakes of the genus Storeria. American Midland Naturalist 31 : 1 84.
80. Uller T, Olsson M. 2008. Multiple paternity in reptiles: patterns and processes. Molecular Ecology 17 : 2566 2580.
81. Ursenbacher S, Erny C, Fumagalli L. 2008. Male reproductive success and multiple paternity in wild, low-density populations of the adder (Vipera berus). Journal of Heredity 100 : 365 370.
82. Utiger U, Helfenberger N, Schätti B, Schmidt C, Ruf M, Ziswiler V. 2002. Molecular systematics and phylogeny of Old and New World ratsnakes, Elaphe auct., and related genera (reptilia, squamata, colubridae). Russian Journal of Herpetology 9 : 105 124.
83. Voris HK, Karns DR, Feldheim KA, Kechavarzi B, Rinehart M. 2008. Multiple paternity in the Oriental-Australian rear-fanged watersnakes (Homolopsidae). Herpetological Conservation and Biology 3 : 88 102.
84. Zaher H. 1999. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubrid hemipenes. Bulletin of the American Museum of Natural History 240 : 1 168.
85. Zar JH. 1999. Biostatistical analysis, 4th edn. Upper Saddle River, NJ : Prentice Hall.