Molecular approaches to the study of parentage, relatedness, and fitness: Practical applications for wild animals

Journal of Wildlife Management

Volumn 69, Issue 4, 2005, Pages 1400-1418

  DeWoody, J Andrew ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Cannibalism; Dispersal; Evolution; Genetics; Genotoxicology; Hybridization; Kinship; Mate choice; Reproductive success; Transgenic

Indexed keywords

MOLECULAR ANALYSIS; POPULATION GENETICS; WILDLIFE MANAGEMENT;

ANIMALIA;

EID: 33645680264     PISSN: 0022541X     EISSN: None     Source Type: Journal    
DOI: 10.2193/0022-541X(2005)69[1400:MATTSO]2.0.CO;2     Document Type: Review

References (150)

1. AITKEN, N., S. SMITH, C. SCHWARZ, AND P. A. MORIN. 2004. Single-nucleotide polymorphism discovery in mammals: a targeted gene approach. Molecular Ecology 13:1423-1431.
2. ALLENDORF, F. W., R. F. LEARY, P. SPRUELL, AND J. K. WENBURG. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution 16:613-622.
3. AMOS, W., J. WORTHINGTON-WILMER, K. FULLARD, T. M. BURG, J. P. CROXALL, D. BLOCH, AND T. COULSON. 2001. The influence of parental relatedness on reproductive success. Proceedings of the Royal Society Series B 268:2021-2027.
4. ARNOLD, M. L. 1997. Natural hybridization and evolution. Oxford University Press, New York, USA.
5. AVISE, J. C. 2004a. Molecular markers, natural history, and evolution. Second edition. Sinauer Press, Sunderland, Massachusetts, USA.
6. _. 2004b. The hope, hype, and reality of genetic engineering. Oxford University Press, New York, USA.
7. _, A. G. JONES, D. WALKER, AND J. A. DEWOODY. 2002. Microsatellite profiles of the genetic mating systems and reproductive natural histories of fishes. Annual Review of Genetics 36:19-45.
8. _, A. J. POWER, AND D. WALKER. 2004. Genetic sex determination, gender identification, and pseudohermaphroditism in the knobbed whelk, Busycon carica (Mollusca: Melongenidae). Proceedings of the Royal Society Series B 271:641-646.
9. BAKER, R. J., J. A. DEWOODY, A. J. WRIGHT, AND R. K. CHESSER. 1999a. On the utility of heteroplasmy in genotoxic studies: an example from Chernobyl. Ecotoxicology 8:301-309.
10. _, K. D. MAKOVA, AND R. K. CHESSER. 1999b. Microsatellites indicate high frequency of multiple paternity in Apodemus (Rodentia). Molecular Ecology 8:107-112.
11. BARTRON, M. L., AND K. T. SCRIBNER. 2004. Temporal comparisons of genetic diversity in Lake Michigan steelhead, Oncorhynchus mykiss, populations: effects of hatchery supplementation. Environmental Biology of Fishes 69:395-407.
12. BEAN, K., W. AMOS, P. P. POMEROY, S. D. TWISS, T. N. COULSON, AND I. L. BOYD. 2004. Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus). Molecular Ecology 13:2365-2370.
13. BEAUMONT, M., E. M. BARRATT, D. GOTTELLI, A. C. KITCHENER, M. J. DANIELS, J. K. PRITCHARD, AND M. W. BRUFORD. 2001. Genetic diversity and introgression in the Scottish wildcat. Molecular Ecology 10:319-336.
14. BENSCH, S., S. ÅKESSON, AND D. E. IRWIN. 2002. The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers. Molecular Ecology 11:2359-2366.
15. BERRY, O., M. D. TOCHER, AND S. D. SARRE. 2004. Can assignment tests measure dispersal? Molecular Ecology 13:551-561.
16. BICKHAM, J. W., S. SANDHU, P. D. N. HEBERT, L. CHIKHI, AND R. ATHWAL. 2000. Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutation Research 463:33-51.
17. BIRKHEAD, T. 2000. Promiscuity. Harvard University Press, Cambridge, Massachusetts, USA.
18. BLOUIN, M. S. 2003. DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends in Ecology and Evolution 18:503-511.
19. _, M. PARSONS, V. LACAILLE, AND S. LOTZ. 1996. Use of microsatellite loci to classify individuals by relatedness. Molecular Ecology 5:393-401.
20. BRANNON, E. L., D. F. AMEND, M. A. CRONIN, J. E. LANNAN, S. LAPATRA, W. J. MCNEIL, R. E. NOBLE, C. E. SMITH, A. J. TALBOT, G. A. WEDEMEYER, AND H. WESTERS. 2004. The controversy about salmon hatcheries. Fisheries 29:12-31.
21. BROHEDE, J., C. R. PRIMMER, A. MØLLER, AND H. ELLEGREN. 2002. Heterogeneity in the rate and pattern of germline mutation at individual microsatellite loci. Nucleic Acids Research 30:1997-2003.
22. BROMHAM, L., AND D. PENNY. 2003. The modern molecular clock. Nature Reviews Genetics 4:216-224.
23. BROTHERTON, P. N. M., J. M. PEMBERTON, P. E. KOMERS, AND G. MALARKY. 1997. Genetic and behavioural evidence of monogamy in a mammal. Proceedings of the Royal Society Series B 264:675-681.
24. BULL, C. M., S. J. B. COOPER, AND B. C. BAGHURST. 1998. Social monogamy and extra-pair fertilization in an Australian lizard Tiliqua rugosa. Behavioral Ecology and Sociobiology 44:63-72.
25. BULL, J. J. 1983. Evolution of sex determining mechanisms. Benjamin/Cummings, Menlo Park, California, USA.
26. CARLING, M. D., P. A. WISEMAN, AND J. A. BYERS. 2003. Microsatellite analysis reveals multiple paternity in a population of wild pronghorn antelopes (Antilocapra americana). Journal of Mammalogy 84:1237-1243.
27. CARVALHO, G. R., AND L. HAUSER. 1998. Advances in the molecular analysis of fish population structure. Italian Journal of Zoology 65S:21-33.
28. CATHEY, J. C., J. W. BICKHAM, AND J. C. PATTON. 1998. Introgressive hybridization and nonconcordant evolutionary history of maternal and paternal lineages in North American deer. Evolution 52:1224-1229.
29. COLTMAN, D. W., P. O'DONOGHUE, J. T. JORGENSON, J. T. HOGG, C. STROBECK, AND M. FESTA-BIANCHET. 2003. Undesirable evolutionary consequences of trophy hunting. Nature 426:655-658.
30. COMER, C. E., J. C. KILGO, G. J. D'ANGELO, T. C. GLENN, AND K. V. MILLER. 2005. Fine-scale genetic structure and social organization in female white-tailed deer. Journal of Wildlife Management 69:332-344.
31. DAVIS, L. M., T. C. GLENN, R. M. ELSEY, H. C. DESSAUER, AND R. H. SAWYER. 2001. Multiple paternity and mating patterns in the American alligator, Alligator mississipiensis. Molecular Ecology 10:1011-1024.
32. DEVLIN, R. H., M. D'ANDRADE, M. UH, AND C. A. BIAGI. 2004. Population effects of growth hormone transgenic coho salmon depend on food availability and genotype by environment interactions. Proceedings of the National Academy of Sciences USA 101:9303-9308.
33. DEWOODY, J. A., AND J. C. AVISE. 2000. Microsatellite variation in animal populations, with special emphasis on marine, freshwater, and anadromous fishes. Journal of Fish Biology 56:461-473.
34. _, AND _. 2001. Genetic perspectives on the natural history of fish mating systems. Journal of Heredity 92:167-172.
35. _, D. E. FLETCHER, S. D. WILKINS, W. S. NELSON, AND J. C. AVISE. 1998. Molecular genetic dissection of spawning, parentage, and reproductive tactics in a population of redbreast sunfish, Lepomis auritus. Evolution 52:1802-1810.
36. _, AND _. 2000a. Biparental care and genetic monogamy in an externally-fertilizing fish, the largemouth bass (Micropterus salmoides). Proceedings of the Royal Society Series B 267:2431-2437.
37. _, AND _. 2000b. Microsatellite analyses of parentage and nest guarding in the tessellated darter (Pisces: Percidae). Copeia 2000: 740-747.
38. _, Y. D. DEWOODY, A. C. FIUMERA, AND J. C. AVISE. 2000c. On the number of reproductives contributing to a half-sib progeny array. Genetical Research (Cambridge) 75:95-105.
39. _, D. E. FLETCHER, S. D. WILKINS, AND J. C. AVISE. 2001. Genetic documentation of filial cannibalism. Proceedings of National Academy of Sciences USA 98:5090-5092.
40. DEYOUNG, R. W., S. DEMARAIS, R. A. GONZALES, R. L. HONEYCUTT, AND K. L. GEE. 2002. Multiple paternity in white-tailed deer (Odocoileus virginianus) revealed by DNA microsatellites. Journal of Mammalogy 83:884-892.
41. DITCHKOFF, S. S., R. L. LOCHMILLER, R. E. MASTERS, S. R. HOOFER, AND R. A. VAN DEN BUSSCHE. 2001. Major histocompatibility complex-associated variation in secondary sexual traits of white-tailed deer: evidence for good-genes advertisement. Evolution 55:616-625.
42. DOBSON, F. S., R. K. CHESSER, J. L. HOOGLAND, D. W. SUGG, AND D. W. FOLTZ. 1997. Do black-tailed prarie dogs minimize inbreeding? Evolution 51:970-978.
43. DUNN, P. O., A. D. AFTON, M. L. GLOUTNEY, AND R. T. ALISAUSKAS. 1999. Forced copulation results in few extrapair fertilizations in Ross's and lesser snow geese. Animal Behaviour 57:1071-1081.
44. EDWARDS, S. V., AND P. W. HEDRICK. 1998. Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends in Ecology and Evolution 13:305-311.
45. ELGAR, M. A., AND B. J. CRESPI. 1992. Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, New York, USA.
46. ELLEGREN, H., L. GUSTAFSSON, AND B. C. SHELDON. 1996. Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proceedings of National Academy of Sciences USA 93:11723-11728.
47. _, G. LINDGREN, C. R. PRIMMER, AND A. P. MOLLER. 1997. Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature 389:593-596.
48. ELLSTRAND, N. C. 2003. Dangerous liasons: when cultivated plants mate with their wild relatives. Johns Hopkins University Press, Baltimore, Maryland, USA.
49. ERLICH, H. A., AND N. ARNHEIM. 1992. Genetic analysis using the polymerase chain reaction. Annual Review of Genetics 26:479-506.
50. EVANS, B. J., J. SUPRIATNA, AND D. J. MELNICK. 2001. Hybridization and population genetics of 2 macaque species in Sulawesi, Indonesia. Evolution 55:1686-1702.
51. FITZSIMMONS, N. N., S. W. BUSKIRK, AND M. H. SMITH. 1995. Population history, genetic variability, and horn growth in bighorn sheep. Conservation Biology 9:314-323.
52. FIUMERA, A. C., B. A. PORTER, G. D. GROSSMAN, AND J. C. AVISE. 2002. Intensive genetic assessment of the mating system and reproductive success in a semi-closed population of the mottled sculpin, Cottus bairdi. Molecular Ecology 11:2367-2377.
53. _, B. A. PORTER, G. LOONEY, M. A. ASMUSSEN, AND J. C. AVISE. 2004. Maximizing offspring production while maintaining genetic diversity in supplemental breeding programs of highly fecund managed species. Conservation Biology 18:94-101.
54. GARANT, D., I. A. FLEMING, S. EINUM, AND L. BERNATCHEZ. 2003. Alternative male life-history tactics as potential vehicles for speeding introgression of farm salmon traits into wild populations. Ecology Letters 6:541-549.
55. GARRIGAN, D., AND P. W. HEDRICK. 2001. Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon. Immunogenetics 53:483-489.
56. GEMMELL, N. J., V. J. METCALF, AND F. W. ALLENDORF. 2004. Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends in Ecology and Evolution 19:238-244.
57. GLAUBITZ, J. C., O. E. RHODES, AND J. A. DEWOODY. 2003. Prospects for inferring pairwise relationships with single nucleotide polymorphisms (SNPs). Molecular Ecology 12:1039-1048.
58. GOOSSENS, B., L. GRAZIANI, L. P. WAITS, E. FARAND, S. MAGNOLON, J. COULON, M.-C. BEL, P. TABERLET, AND D. ALLAINE. 1998. Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behavioural Ecology and Sociobiology 43:281-288.
59. GOTTELLI, D., C. SILLEROZUBIRI, G. D. APPLEBAUM, M. S. ROY, D. J. GIRMAN, J. GARCIA-MORENO, E. A. OSTRANDER, AND R. K. WAYNE. 1994. Molecular genetics of the most endangered canid: the Ethiopian wolf, Canis simensis. Molecular Ecology 3:301-312.
60. GRIFFITH, S. C., I. P. F. OWENS, AND K. A. THUMAN. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology 11:2195-2212.
61. GROB, B., L. A. KNAPP, R. D. MARTIN, AND G. ANZENBERGER. 1998. The major histocompatibility complex and mate choice: inbreeding avoidance and selection of good genes. Experimental and Clinical Immunogenetics 15:119-129.
62. HALLERMAN, E. M., AND A. R. KAPUSCINSKI. 1995. Incorporating risk assessment and risk management into public policies on genetically modified finfish and shellfish. Aquaculture 137:9-17.
63. HAYNIE, M. L., R. A. VAN DEN BUSSCHE, J. L. HOOGLAND, AND D. A. GILBERT. 2003. Parentage, multiple paternity, and breeding success in Gunnison's and Utah prairie dogs. Journal of Mammalogy 84:1244-1253.
64. HEDRICK, P. W. 2001. Invasion of transgenes from salmon or other genetically modified organisms into natural populations. Canadian Journal of Fisheries and Aquatic Sciences 58:841-844.
65. _, D. HEDGECOCK, S. HAMELBERG, AND S. J. CROCI. 2000. The impact of supplementation in winter-run chinook salmon on effective population size. Journal of Heredity 91:112-116.
66. _, R. N. LEE, AND C. BUCHANAN. 2003. Canine parvovirus enteritis, canine distemper, and major histocompatibility complex genetic variation in Mexican wolves. Journal of Wildlife Diseases 39:909-913.
67. HOFFMAN, J. I., I. L. BOYD, AND W. AMOS. 2003. Male reproductive strategy and the importance of maternal status in the antarctic fur seal Arctocephalus gazella. Evolution 57:1917-1930.
68. HONEYCUTT, R. L. 1992. Naked mole-rats. American Scientist 80:43-54.
69. HOWARD, R. D., J. A. DEWOODY, AND W. MUIR. 2004. Alternative mating tactics may halt a Trojan gene despite transgenic mating advantage. Proceedings of the National Academy of Sciences USA 101:2934-2938.
70. HOWE, H. F. 1977. Sex-ratio adjustment in common grackle. Science 198:744-746.
71. IBARGUCHI, G., G. J. GISSING, A. J. GASTON, P. T. BOAG, AND V. L. FRIESEN. 2004. Male-biased mutation rates and the overestimation of extrapair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia, Alcidae). Journal of Heredity 95:205-216.
72. JONES, A. G., AND W. R. ARDEN. 2003. Methods of parentage analysis in natural populations. Molecular Ecology 12:2511-2523.
73. _, E. M. ADAMS, AND S. J. ARNOLD. 2002. Topping off: a mechanism of first-male sperm precedence in a vertebrate. Proceedings of the National Academy of Sciences USA 99:2078-2081.
74. _, C. KVARNEMO, G. I. MOORE, L. W. SIMMONS, AND J. C. AVISE. 1998a. Microsatellite evidence for monogamy and sex-biased recombination in the western Australian seahorse Hippocampus angustus. Molecular Ecology 7:1497-1505.
75. _, S. ÖSTLUND-NILSSON, AND J. C. AVISE. 1998b. A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution 52:848-858.
76. _, G. ROSENQVIST, A. BERGLUND, AND J. C. AVISE. 1999. Clustered microsatellite mutations in the pipefish Sygnathus typhle. Genetics 152:1057-1063.
77. KELLER, L. F., AND D. M. WALLER. 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17:230-241.
78. KING, R. B., W. B. MILSTEAD, H. L. GIBBS, M. R. PROSSER, G. M BURGHARDT, AND G. F. MCCRACKEN. 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.
79. KOEHN, R. K., AND T. J. HILBISH. 1987. The adaptive importance of genetic variation. American Scientist 75:134-141.
80. KOMDEUR, J., S. DAAN, J. TINBERGEN, AND C. MATEMAN. 1997. Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature 385:522-525.
81. _. 2003. Daughters on request: about helpers and egg sexes in the Seychelles warbler. Proceedings of the Royal Society Series B 270:3-11.
82. KRUUK, L. E. B. 2004. Estimating genetic parameters in natural populations using the 'animal model.' Philosophical Transactions of the Royal Society of London, Series B 359:873-890.
83. KUKEKOVA, A. V., L. N. TRUT, I. N. ISKINA, A. V. KHARLAMOVA, S. G. SKIKHEVICH, E. F. KIRKNESS, G. D. AGUIRRE, AND G. M. ACLAND. 2004. A marker set for construction of a genetic map of the silver fox (Vulpes vulpes). Journal of Heredity 95:185-194.
84. KWOK, P. 2001. Methods for genotyping single nucleotide polymorphisms. Annual Review of Genomics and Human Genetics 2:235-258.
85. 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). Proceedings of the Royal Society Series B 268, 1279-1285.
86. LEE, P. L. M., AND G. C. HAYS. 2004. Polyandry in a marine turtle: females make the best of a bad job. Proceedings of the National Academy of Sciences USA 101:6530-6535.
87. LIM, M. M., Z. WANG, D. E. OLAZÁBAL, X. REN, E. F. TERWILLIGER, AND L. J. YOUNG. 2004. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 249:754-757.
88. LINDSTRÖM, K. 2000. The evolution of filial cannibalism and female mate choice strategies as resolutions to sexual conflict in fishes. Evolution 54:617-627.
89. LYNCH, M., AND K. RITLAND. 1999. Estimation of pairwise relatedness with molecular markers. Genetics 152:1753-1766.
90. MANK, J. E., J. E. CARLSON, AND M. C. BRITTINGHAM. 2004. A century of hybridization: decreasing genetic distance between American black ducks and mallards. Conservation Genetics 5:395-403.
91. MARGALIDA, A., J. BERTRAN, J. BOUDET, AND R. HEREDIA. 2004. Hatching asynchrony, sibling aggression and cannibalism in the Bearded Vulture Gypaetus barbatus. Ibis 146:386-393.
92. MARGULIS, L. 1981. Symbiosis in cell evolution: life and its environment in the early earth. W. H. Freeman, San Fransisco, California, USA.
93. MATTSON, D. J., R. R. KNIGHT, AND B. M. BLANCHARD. 1992. Cannibalism and predation on black bears by grizzly bears in the Yellowstone ecosystem, 1975-1990. Journal of Mammalogy 73:422-425.
94. MCGINNITY, P., P. PRODOHL, A. FERGUSON, R. HYNES, N. O. MAOILEIDIGH, N. BAKER, D. COTTER, D. O'HEA, D. COOKE, G. ROGAN, J. TAGGART, AND T. CROSS. 2003. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society Series B 270:2443-2450.
95. MCKELVEY, K. S., AND M. K. SCHWARTZ. 2004. Genetic errors associated with population estimation using noninvasive molecular tagging: problems and new solutions. Journal of Wildlife Management 68:439-448.
96. MCLUCKIE, A. M., T. LAMB, C. R. SCHWALBE, AND R. D. MCCORD. 1999. Genetic and morphometric assessment of an unusual tortoise (Gopherus agassizii) population in the Black Mountains of Arizona. Journal of Herpetology 33:36-44.
97. MILLER, C. R., AND L. P. WAITS. 2003. The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): implications for conservation. Proceedings of the National Academy of Sciences USA 100:4334-4339.
98. MUIR, W. M., AND R. D. HOWARD. 1999. Possible ecological risks of transgenic organism release when transgenes affect mating success: sexual selection and the Trojan gene hypothesis. Proceedings of the National Academy of Sciences USA 96:13853-13856.
99. _, AND _. 2002. Assessment of possible ecological risks and hazards of transgenic fish with implications for other sexually reproducing organisms. Transgenic Research 11:101-114.
100. MYERS, E. M., AND K. R. ZAMUDIO. 2004. Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success. Molecular Ecology 13:1951-1963.
101. OLSSON, M., T. MADSEN, J. NORDBY, E. WAPSTRA, B. UJVARI, AND H. WITTSELL. 2003. Major histocompatibility complex and mate choice in sand lizards. Proceedings of the Royal Society Series B 270:S254-S256.
102. PAETKAU, D. 2004. The optimal number of markers in genetic capture-mark-recapture studies. Journal of Wildlife Management 68:449-452.
103. _, W. CALVERT, I. STIRLING, AND C. STROBECK. 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4:347-354.
104. PAGE K. S., K. T. SCRIBNER, AND M. BURNHAM-CURTIS. 2004. Genetic diversity of wild and hatchery lake trout populations: Relevance for management and restoration in the Great Lakes. Transactions of the American Fisheries Society 133:674-691.
105. PEARSE, D. E., M. ECKERMAN, F. J. JANZEN, AND J. C. AVISE. 2001. A genetic analogue of "mark-recapture" methods for estimating population size: an approach based on molecular parentage assessments. Molecular Ecology 10:2711-2718.
106. _, F. J. JANZEN, AND J. C. AVISE. 2002. Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysems picta) in nature. Behavioral Ecology and Sociobiology 51:164-171.
107. ST: analysis of population genetic data for conservation. Conservation Genetics 5:585-602.
108. PENN, D. J., K. DAMJANOVICH, AND W. K. POTTS. 2002. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proceedings of the National Academy of Sciences USA 99:11260-11264.
109. PERRY, W. L., J. L. FEDER, G. DWYER, AND D. M. LODGE. 2001. Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution 55:1153-1166.
110. PFENNIG, D. W. 1999. Cannibalistic tadpoles that pose the greatest threat to kin are the most likely to discriminate kin. Proceedings of the Royal Society Series B 266:57-61.
111. _, AND J. P. COLLINS. 1993. Kinship affects morphogenesis in cannibalistic salamanders. Nature 362:836-838.
112. POTTS, W. K., C. J. MANNING, AND E. K. WAKELAND. 1991. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352:619-621.
113. PRIMMER, C. R., H. ELLEGREN, N. SAINO, AND A. P. MØLLER. 1996. Directional evolution in germline microsatellite mutations. Nature Genetics 13:391-393.
114. PRUGNOLLE, F., AND T. DE MEEUS. 2002. Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161-165.
115. QUELLER, D. C., AND K. F. GOODNIGHT. 1989. Estimating relatedness using genetic markers. Evolution 43:258-275.
116. REEVE, H. K., D. F. WESTNEAT, W. A. NOON, P. W. SHERMAN, AND C. F. AQUADRO. 1990. DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proceedings of the National Academy of Sciences USA 87:2496-2500.
117. RICHARDSON, B. J., R. A. HAYES, S. H. WHEELER, AND M. R. YARDIN. 2002a. Social structures, genetic structures, and dispersal strategies in Australian rabbit (Oryctolagus cuniculus) populations. Behavioral Ecology and Sociobiology 51:113-121.
118. RICHARDSON, D. S., T. BURKE, AND J. KOMDEUR. 2002b. Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers. Evolution 56:2313-2321.
119. RITLAND, K. 2000. Marker-inferred relatedness as a tool for detecting heritability in nature. Molecular Ecology 9:1195-1204.
120. ROOTES, W. L., AND R. H. CHABRECK. 1993. Cannibalism in the American alligator. Herpetologica 49:99-107.
121. ROSSITER, S. J., G. JONES, R. D. RANSOME, AND E. M. BARRATT. 2000. Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proceedings of the Royal Society Series B 267:545-551.
122. RUDNICK, J. A., T. E. KATZNER, E. A. BRAGIN, O. E. RHODES, AND J. A. DEWOODY. 2005. Using naturally shed feathers for individual identification, genetic parentage analyses, and population monitoring in an endangered eastern imperial eagle (Aquila heliaca) population from Kazakhstan. Molecular Ecology 14:2959-2967.
123. SCHŪLKE, O., P. M. KAPPELER, AND H. ZISCHLER. 2004. Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behavioral Ecology and Sociobiology 55:293-301.
124. SCRIBNER, K. T., AND T. D. BOWMAN. 1998. Microsatellites identify depredated waterfowl remains from glaucous gull stomachs. Molecular Ecology 7:1401-1405.
125. _, K. S. PAGE, AND M. L. BARTRON. 2000. Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries 10:293-323.
126. SELANDER, R. K. 1976. Genic variation in natural populations. Pages 21-45 in F. J. Ayala, editor. Molecular evolution. Sinauer Press, Sunderland, Massachusetts, USA.
127. SEMPLE, K., R. K. WAYNE, AND R. M. GIBSON. 2001. Microsatellite analysis of female mating behaviour in lek-breeding sage grouse. Molecular Ecology 10:2043-2048.
128. SHELDON, B. C., J. MERILA, G. LINDGREN, AND H. ELLEGREN. 1998. Gender and environmental sensitivity in nestling collared flycatchers. Ecology 79:1939-1948.
129. SINERVO, B., AND K. R. ZAMUDIO. 2001. The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes. Journal of Heredity 92:198-205.
130. SOMERS, C. M., B. E. MCCARRY, F. MALEK, AND J. S. QUINN. 2004. Reduction of particulate air pollution lowers the risk of heritable mutations in mice. Science 304:1008-1010.
131. SORIN, A. B. 2004. Paternity assignment for white-tailed deer (Odocoileus virginianus): mating across age classes and multiple paternity. Journal of Mammalogy 85:356-362.
132. STOCKLEY, P., J. B. SEARLE, D. W. MACDONALD, AND C. S. JONES. 1993. Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proceedings of the Royal Society Series B 254:173-179.
133. SYMONDSON, W. O. C. 2002. Molecular identification of prey in predator diets. Molecular Ecology 11:627-641.
134. TABERLET, P., L. P. WAITS, AND G. LUIKART. 1999. Noninvasive genetic sampling: look before you leap. Trends in Ecology and Evolution 14:323-327.
135. TRIANT, D. A., R. M. PACE, III, AND M. STINK. 2005 Abundance, genetic diversity and conservation of Louisiana black bears (Ursus americanus luteolus) as detected through noninvasive sampling. Conservation Genetics 5:647-659.
136. TURNER, G. F. 1999. What is a fish species? Reviews in Fish Biology and Fisheries 9:281-297.
137. VALERA, F., H. HOI, AND A. KRISTIN. 2003. Male shrikes punish unfaithful females. Behavioral Ecology 14:403-408.
138. VIEITES, D. R., S. NIETO-ROMAN, M. BARLUENGA, A. PALANCA, M. VENCES, AND A. MEYER. 2004. Post-mating clutch piracy in an amphibian. Nature 431:305-308.
139. WAITS, L. P., G. LUIKART, AND P. TABERLET. 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10:249-256.
140. WALLS, S. C., AND A. R. BLAUSTEIN. 1995. Larval marbled salamanders, Ambystoma opacum, eat their kin. Animal Behaviour 50:537-545.
141. WASER, P. M., AND C. STROBECK. 1998. Genetic signatures of interpopulation dispersal. Trends in Ecology and Evolution 13:43-44.
142. WEDEKIND, C., AND S. FÜRI. 1997. Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proceedings of the Royal Society Series B 264:1471-1479.
143. WICKLIFFE, J. K., R. K. CHESSER, B. E. ROGERS, AND R. J. BAKER. 2002. Assessing the genotoxicity of chronic environmental irradiation by using mitochondrial DNA heteroplasmy in the bank vole (Clethrionomys glareolus) at Chornobyi, Ukraine. Environmental Toxicology and Chemistry 21:1249-1254.
144. WILLIAMS, B. K., J. D. NICHOLS, AND M. J. CONROY. 2002. Analysis and management of animal populations. Academic Press, New York, USA.
145. WILLIAMS, C. L., T. L. SERFASS, R. COGAN, AND O. E. RHODES. 2002. Microsatellite variation in the reintroduced Pennsylvania elk herd. Molecular Ecology 11:1299-1310.
146. WINTERS, J. B., AND P. M. WASER. 2003. Gene dispersal and outbreeding in a philopatric mammal. Molecular Ecology 12:2251-2259.
147. WRIGHT, S. 1978. Evolution and the genetics of populations, volume IV: variability within and among natural populations. University of Chicago Press, Chicago, Illinois, USA.
148. YAUK, C. 1998. Monitoring for induced heritable mutations in natural populations: application of minisatellite DNA screening. Mutation Research 411:1-10.
149. ZAMUDIO, K. R., AND B. SINERVO. 2000. Polygyny, mateguarding, and posthumous fertilization as alternative male mating strategies. Proceedings of the National Academy of Sciences USA 97:14427-14432.
150. ZHANG, J. Z., D. M. WEBB, AND O. PODLAHA. 2002. Accelerated protein evolution and origins of human-specific features: FOXP2 as an example. Genetics 162:1825-1835.