Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris

Evolution

Volumn 58, Issue 10, 2004, Pages 2332-2342

  Feldheim, Kevin A ^a,c   Gruber, Samuel H ^b   Ashley, Mary V ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF MIAMI   (United States)

^c FIELD MUSEUM OF NATURAL HISTORY   (United States)

Author keywords

Genotype reconstruction; Lemon shark; Microsatellites; Parentage assignment; Polyandry; Relatedness

Indexed keywords

EVOLUTION; GENETIC ANALYSIS; PHILOPATRY; POLYANDRY; REPRODUCTIVE STRATEGY; SHARK;

CHONDRICHTHYES; CITRUS LIMON; ELASMOBRANCHII; NEGAPRION BREVIROSTRIS; TRANSPOSONS;

EID: 7544226470     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01607.x     Document Type: Article

References (54)

1. Arnqvist, G., and T. Nillson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60: 145-164.
2. Bentzen, P., J. B. Olsen, J. E. McLean, T. R. Seamons, and T. P. Quinn. 2001. Kinship analysis of Pacific salmon: insights into mating, homing, and timing of reproduction. J. Hered. 92: 127-136.
3. Bigelow, H. B., and W. C. Schroeder. 1948. Fishes of the western North Atlantic. Mem. Sears Found. Mar. Res. 1:59-545.
4. Blouin, M. S., M. Parsons, V. Lacaille, and S. Lotz. 1996. Use of microsatellite loci to classify individuals by relatedness. Mol. Ecol. 5:393-401.
5. Branstetter, S. 1987. Age, growth, and reproductive biology of the silky shark, Carcharhinus falciformis, and the scalloped hammerhead, Sphyrna lewini, from the northwestern Gulf of Mexico. Environ. Biol. Fish. 19:161-173.
6. Brown, C. A., and S. H. Gruber. 1988. Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra. Copeia 1988:747-753.
7. Carrier, J. C., H. L. Pratt, and L. Martin. 1994. Group reproductive behavior in free-living nurse sharks, Ginglymostoma cirratum. Copeia 1994:646-656.
8. Castro, J. I. 1996. Biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bull. Mar. Sci. 59: 508-522.
9. _. 2000. The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands. Environ. Biol. Fish. 58:1-22.
10. Castro, J. I., P. M. Bubucis, and N. A. Overstrom. 1988. The reproductive biology of the chain dogfish, Scyliorhinus retifer. Copeia 1988:740-746.
11. Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41-47.
12. Compagno, L. J. V. 1984. FAO species catalogue: sharks of the world. Food and Agriculture Organization of the United Nations, Rome.
13. Dawkins, R., and T. R. Carlisle. 1976. Parental investment, mate desertion and a fallacy. Nature 262:131-133.
14. DeWoody, J. A., D. E. Fletcher, S. D. Wilkins, W. S. Nelson, and J. C. Avise. 2000. Genetic monogamy and biparental care in an externally fertilizing fish, the largemouth bass (Micropterus salmoides). Proc. R. Soc. Lond. B 267:2431-2437.
15. Evans, J. P., and A. E. Magurran. 2000. Multiple benefits of multiple mating in guppies. Proc. Natl. Acad. Sci. USA 97:10074-10076.
16. Feldheim, K. A., S. H. Gruber, and M. V. Ashley. 2001a. Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia 2001:781-786.
17. _. 2001b. Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Mol. Ecol. 10:295-303.
18. _. 2002. Breeding biology of lemon sharks at a tropical nursery lagoon. Proc. R. Soc. Lond. B 269:1655-1662.
19. Goodnight, K. F., and D. C. Queller. 1999. Computer software for performing likelihood tests of pedigree relationships using genetic markers. Mol. Ecol. 8:1231-1234.
20. Gross, M. R., and R. Shine. 1981. Parental care and mode of fertilization in ectothermic vertebrates. Evolution 35:775-793.
21. Gruber, S. H., and W. Parks. 2002. Mega-resort development on Bimini: Sound economics or environmental disaster? Bahamas J. Sci. 9:2-18.
22. Gruber, S. H., J. R. C. de Marignac, and J. M. Hoenig. 2001. Survival of juvenile lemon sharks at Bimini, Bahamas, estimated by mark-depletion experiments. Trans. Am. Fish. Soc. 130: 376-384.
23. Harvey, P. H., and R. M. May. 1989. Out for the sperm count. Nature 337:508-509.
24. Jennions, M. D., and M. Petrie. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75:21-64.
25. Joung, S. J., and C. T. Chen. 1995. Reproduction in the sandbar shark, Carcharhinus plumbeus, in the waters off Northeastern Taiwan. Copeia 1995:659-665.
26. Keller, L., and H. K. Reeve. 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv. Stud. Behav. 24:291-315.
27. Kichler, K., M. T. Holder, S. K. Davis, R. Marquez-M., and D. W. Owens. 1999. Detection of multiple paternity in the Kemp's ridley sea turtle with limited sampling. Mol. Ecol. 8:819-830.
28. Landry, C., D. Garant, P. Duchesne, and L. Bernatchez. 2001. "Good genes as heterozygosity": the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. Lond. B 268:1279-1285.
29. Manire, C. A., and S. H. Gruber. 1993. A preliminary report on the rate of natural mortality of juvenile lemon sharks, Negaprion brevirostris. NOAA Tech. Rpt. NMFS 115:65-71.
30. Marshall, T. C., J. Slate, J. E. B. Kruuk, and J. M. Pemberton. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7:639-655.
31. Morrissey, J. F., and S. H. Gruber. 1993. Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993:425-434.
32. Ohta, Y., K. Okamura, E. C. McKinney, S. Bartl, K. Hashimoto, and M. F. Flajnik. 2000. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc. Natl. Acad. Sci. USA 97:4712-4717.
33. Pardini, A. T., C. S. Jones, L. R. Noble, B. Kreiser, H. Malcolm, B. D. Bruce, J. D. Stevens, G. Cliff, M. C. Scholl, M. Francis, C. A. J. Duffy, and A. P. Martin. 2001. Sex-biased dispersal of great white sharks. Nature 412:139-140.
34. Petrie, M., and B. Kempenaers. 1998. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol. Evol. 13:52-58.
35. Pratt, H. L. J. 1993. The storage of spermatozoa in the oviducal glands of western North Atlantic sharks. Environ. Biol. Fish. 38:139-149.
36. Pratt, H. L. J., and J. C. Carrier. 2001. A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ. Biol. Fish 60:157-188.
37. Queller, D. C., and K. F. Goodnight. 1989. Estimating relatedness using genetic markers. Evolution 43:258-275.
38. Ridley, M. 1993. Clutch size and mating frequency in parasitic Hymenoptera. Am. Nat. 142:893-910.
39. Saville, K. J., A. M. Lindley, E. G. Maries, J. C. Carrier, and H. L. Pratt. 2002. Multiple paternity in the nurse shark, Ginglymostoma cirratum. Environ. Biol. Fish 63:347-351.
40. Shrey, A. W., and E. J. Heist. 2003. Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Can. J. Fish. Aquat. Sci. 60:670-675.
41. Simmons, L. W. 2003. The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sex-sperm hypothesis. J. Evol. Biol. 16:624-634.
42. Strausberger, B. M., and M. V. Ashley. 2003. Breeding biology of brown-headed cowbirds characterized by parent-offspring and sib-group reconstruction. Auk 120:433-445.
43. Sundström, L. F., S. H. Gruber, S. M. Clermont, J. P. S. Correia, J. R. C. de Marignac, J. F. Morrissey, C. R. Lowrance, L. Thomassen, and M. T. Oliveira. 2001. Review of elasmobranch behavioral studies using ultrasonic telemetry with special reference to the lemon shark, Negaprion brevirostris, around Bimini Islands, Bahamas. Environ. Biol. Fish. 60:225-250.
44. Sunnucks, P., and D. F. Hales. 1996. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol. Biol. Evol. 13: 510-524.
45. Tregenza, T., and N. Wedell. 2000. Genetic incompatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9: 1013-1027.
46. _. 2002. Polyandrous females avoid costs of inbreeding. Nature 415:71-73.
47. Watson, P. J. 1991. Multiple paternity as genetic bet-hedging in female sierra dome spiders (Linyphia litigiosa: Lynyphiidae). Anim. Behav. 41:343-360.
48. Williams, G. C. 1975. Sex and evolution. Princeton Univ. Press, Princeton, NJ.
49. Worthingham Wilmer, J., P. J. Allen, P. P. Pomeroy, S. D. Twiss, and W. Amos. 1999. Where have all the fathers gone? An extensive analysis of paternity in the grey seal (Halichoerus grypus). Mol. Ecol. 8:1417-1430.
50. Yasui, Y. 1998. The "genetic benefits" of female multiple mating reconsidered. Trends Ecol. Evol. 13:246-250.
51. Zeh, J. A., and D. W. Zeh. 1996. The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B. 263:1711-1717.
52. _. 1997. The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc. R. Soc. Lond. B. 264:69-75.
53. _. 2001. Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61:1051-1063.
54. _. 2003. Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929-950.