High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence

Molecular Ecology

Volumn 17, Issue 10, 2008, Pages 2531-2543

  Sefc, Kristina M ^a   Mattersdorfer, Karin ^a   Sturmbauer, Christian ^a   Koblmüller, Stephan ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

Cichlidae; Cuckoldry; Lake Tanganyika; Lamprologini; Multiple paternity; Reproduction

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; CICHLID; FEMALE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; MALE; PATERNAL BEHAVIOR; PHYSIOLOGY;

ANIMALS; CICHLIDS; FEMALE; GENOTYPE; MALE; MICROSATELLITE REPEATS; PATERNAL BEHAVIOR; POLYMORPHISM, GENETIC;

ANIMALIA; CICHLIDAE; LAMPROLOGINI; VARIABILICHROMIS MOORII;

EID: 43049131445     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2008.03763.x     Document Type: Article

References (96)

1. Adams EM, Jones AG, Arnold SJ (2005) Multiple paternity in a natural population of a salamander with long-term sperm storage. Molecular Ecology, 14, 1803 1810.
2. Amundsen T (2003) Fishes as models in studies of sexual selection and parental care. Journal of Fish Biology, 63 (Suppl. A 17 52.
3. Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annual Reviews of Genetics, 36, 19 45.
4. Awata S, Munehara H, Kohda M (2005) Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behavioral Ecology and Sociobiology, 58, 506 516.
5. Awata S, Takeuchi H, Kohda M (2006) The effect of body size on mating system and parental roles in a biparental cichlid fish (Julidochromis transcriptus): a preliminary laboratory experiment. Journal of Ethology, 24, 125 132.
6. Becher SA, Magurran AE (2004) Multiple mating and reproductive skew in Trinidadian guppies. Proceedings of the Royal Society B: Biological Sciences, 271, 1009 1014.
7. Blumer LS (1982) A bibliography and categorization of bony fishes exhibiting parental care. Zoological Journal of the Linnean Society, 75/76, 1 22.
8. Bouwman KM, Lessells CM, Komdeur J (2005) Male reed buntings do not adjust parental effort in relation to extrapair paternity. Behavioral Ecology, 16, 499 506.
9. Bretman A, Tregenza T (2005) Measuring polyandry in wild populations: a case study using promiscuous crickets. Molecular Ecology, 14, 2169 2179.
10. Carleton KL, Streelman JT, Lee B-Y, Garnhart N, Kidd M, Kocher TD (2002) Rapid isolation of CA microsatellites from the tilapia genome. Animal Genetics, 33, 140 144.
11. Chuang-Dobbs HC, Webster MS, Holmes RT (2001) Paternity and parental care in the black-throated blue warbler, Dendroica caerulescens. Animal Behaviour, 62, 83 92.
12. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology, 10, 1075 1086.
13. DeWoody JA, Avise JC (2001) Genetic perspectives on the natural history of fish mating systems. Journal of Heredity, 92, 167 172.
14. DeWoody JA, Fletcher DE, Wilkins SD, Nelson WS, Avise JC (1998) Molecular genetic dissection of spawning, parentage, and reproductive tactics in a population of redbreast sunfish, Lepomis auritus. Evolution, 52, 1802 1810.
15. DeWoody JA, DeWoody YD, Fiumera AC, Avise JC (2000a) On the number of reproductives contributing to a half-sib progeny array. Genetical Research, 75, 95 105.
16. DeWoody JA, Fletcher DE, Mackiewicz M, Wilkins SD, Avise JC (2000b) The genetic mating system of spotted sunfish (Lepomis punctatus): mate numbers and the influence of male reproductive parasites. Molecular Ecology, 9, 2119 2128.
17. DeWoody JA, Fletcher DE, Wilkins SD, Nelson WS, Avise JC (2000c) Genetic monogamy and biparental care in an externally fertilizing fish, the largemouth bass (Micropterus salmoides). Proceedings of the Royal Society B: Biological Sciences, 267, 2431 2437.
18. Dierkes P, Taborsky M, Kohler U (1999) Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behavioral Ecology, 10, 510 515.
19. Dierkes P, Heg D, Taborsky M, Skubic E, Achmann R (2005) Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecology Letters, 8, 968 975.
20. Dixon A, Ross D, O'Malley SLC, Burke T (1994) Paternal investment inversely related to degree of extra-pair paternity in the reed bunting. Nature, 371, 698 700.
21. Duftner N, Sefc KM, Koblmüller S et al 2006) Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika. Molecular Ecology, 15, 2381 2395.
22. Egger B, Obermüller B, Phiri H, Sturmbauer C, Sefc KM (2006) Monogamy in the maternally mouthbrooding Lake Tanganyika cichlid fish Tropheus moorii. Proceedings of the Royal Society B: Biological Sciences, 273, 1797 1802.
23. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215 223.
24. Felsenstein J (1989) phylip- Phylogeny inference package. Cladistics, 5, 164 166.
25. Fiumera AC, Porter BA, Grossman GD, Avise JC (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.
26. Gardner MG, Bull CM, Cooper SJB (2002) High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii. Molecular Ecology, 11, 1787 1794.
27. Goodwin NB, Balshine-Earn S, Reynolds JD (1998) Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society B: Biological Sciences, 265, 2265 2272.
28. Griffiths SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology, 11, 2195 2212.
29. Gross MR (2005) The evolution of parental care. Quarterly Review of Biology, 80, 37 45.
30. Hain TJA, Neff BD (2007) Multiple paternity and kin recognition mechanisms in a guppy population. Molecular Ecology, 16, 3938 3946.
31. Heg D, Bachar Z, Taborsky M (2005) Cooperative breeding and group structure in the Lake Tangayika cichlid Neolamprologus savoryi. Ethology, 111, 1017 1043.
32. Herbinger CM (2005) pedigree Help Manual. Department of Mathematics and Statistics, Dalhousie University, Halifax, Nova Scotia, Canada. Available from URL: http://herbinger.biology.dal.ca:5080/Pedigree.
33. Herbinger CM, O'Reilly PT, Verspoor E (2006) Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers. Molecular Ecology, 15, 2261 2275.
34. Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends in Ecology & Evolution, 5, 135 140.
35. Jones AG (2005) gerud 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parentage. Molecular Ecology Notes, 5, 708 711.
36. Jones AG, Avise JC (1997) Microsatellite analysis of maternity and the mating system in the Gulf pipefish Syngnathus scovelli, a species with male pregnancy and sex-role reversal. Molecular Ecology, 6, 203 213.
37. Jones AG, Kvrnemo C, Moore GI, Simmons LW, Avise JC (1998a) Microsatellite evidence for monogamy and sex-biased recombination in the Western Australian seahorse Hippocampus angustus. Molecular Ecology, 7, 1497 1505.
38. Jones AG, Östlund-Nilsson S, Avise JC (1998b) A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution, 52, 848 858.
39. Jones AG, Walker D, Kvarnemo C, Lindström K, Avise JC (2001a) How cuckoldry can decrease the opportunity for sexual selection: data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus. Proceedings of the National Academy of Sciences, USA, 98, 9151 9156.
40. Jones AG, Walker D, Lindström K, Kvarnemo C, Avise JC (2001b) Surprising similarity of sneaking rates and genetic mating patterns in two populations of sand goby experiencing disparate sexual selection regimes. Molecular Ecology, 10, 461 469.
41. Karino K (1997) Influence of brood size and offspring size on parental investment in a biparental cichlid fish, Neolamprologus moorii. Journal of Ethology, 15, 39 43.
42. Karino K (1998) Depth-related differences in territory size and defense in the herbivorous cichlid, Neolamprologus moorii, in Lake Tanganyika. Ichthyological Research, 45, 89 94.
43. Katoh R, Munehara H, Kohda M (2005) Alternative male mating tactics of the substrate brooding cichlid Telmatochromis temporalis in Lake Tanganyika. Zoological Science, 22, 555 561.
44. Keenleyside MHA (1991) Parental care. In : Cichlid Fishes - Behaviour, Ecology and Evolution (ed. Keenleyside MHA pp. 191 208. Chapman & Hall, London, UK.
45. Kellogg KA, Markert JA, Stauffer JRJ, Kocher TD (1995) Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proceedings of the Royal Society B: Biological Sciences, 260, 79 84.
46. Kellogg KA, Markert JA, Stauffer JRJ, Kocher TD (1998) Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid. Behavioral Ecology, 9, 309 312.
47. Koblmüller S, Duftner N, Sefc KM et al 2007) Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika - the result of repeated introgressive hybridization. BMC Evolutionary Biology, 7, 7.
48. Kuwamura T (1992) Overlapping territories of Pseudosimochromis curvifrons males and other herbivorous cichlid fishes in Lake Tanganyika. Ecological Research, 7, 43 53.
49. Kuwamura T (1997) The evolution of parental care and mating systems among Tanganyikan cichlids. In : Fish Communities in Lake Tanganyika (eds Kawanabe H, Hori M, Nagoshi M pp. 57 86. Kyoto University Press, Kyoto, Japan.
50. Kvarnemo C, Moore GI, Jones AG, Nelson WS, Avise JC (2000) Monogamous pair bonds and mate switching in the Western Australian seahorse Hippocampus subelongatus. Journal of Evolutionary Biology, 13, 882 888.
51. Kvarnemo C, Moore GI, Jones AG (2007) Sexually selected females in the monogamous Western Australian seahorse Hippocampus subelongatus. Proceedings of the Royal Society B: Biological Sciences, 274, 521 525.
52. Largiadér CR, Fries V, Bakker TCM (2001) Genetic analysis of sneaking and egg-thievery in a natural population of the three-spined stickleback (Gasterosteus aculeatus L.). Heredity, 86, 459 468.
53. Liebgold EB, Cabe PR, Jaeger RG, Leberg PL (2006) Multiple paternity in a salamander with socially monogamous behaviour. Molecular Ecology, 15, 4153 4160.
54. Luo J, Sanetra M, Schartl M, Meyer A (2005) Strong reproductive skew among males in the multiply mated swordtail Xiphophorus multilineatus (Teleostei). Journal of Heredity, 96, 346 355.
55. Mackiewicz M, Fletcher DE, Wilkins SD, DeWoody JA, Avise JC (2002) A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Molecular Ecology, 11, 1877 1883.
56. Matsumoto K, Kohda M (2007) Male foraging avoidance in female feeding territories in a harem polygynous cichlid in Lake Tanganyika. Journal of Ethology, 25, 21 27.
57. McCoy EE, Jones AG, Avise JC (2001) The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally. Molecular Ecology, 10, 1793 1800.
58. McKaye KR, McKaye NM (1977) Communal care and kidnapping of young by parental cichlids. Evolution, 31, 674 681.
59. Minch E (1997) microsat vs 1.5d. Microsat 1.5d. Department of Genetics, University of Stanford, Stanford, California. Available from URL: http://hpgl.stanford.edu/projects/microsat/.
60. Morley JI, Balshine S (2002) Faithful fish: territory and mate defense favour monogamy in an African cichlid fish. Behavioural Ecology and Sociobiology, 52, 326 331.
61. Morley JI, Balshine S (2003) Reproductive biology of Eretmodus cyanostictus, a cichlid fish from Lake Tanganyika. Environmental Biology of Fishes, 66, 169 179.
62. Myers EM, Zamudio KR (2004) Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success. Molecular Ecology, 13, 1951 1963.
63. Neff BD (2001) Genetic paternity analysis and breeding success in bluegill sunfish (Lepomis macrochirus). Journal of Heredity, 92, 111 119.
64. Neff BD (2003) Decisions about parental care in response to perceived paternity. Nature, 422, 716 719.
65. Ochi H, Hata H, Hori M (2007) Advantage of harmlessness in gaining preferential access to a heterospecific territory. Journal of Fish Biology, 71, 399 410.
66. Östlund-Nilsson S (2002) Does paternity or paternal investment determine the level of parental care and does female choice explain egg stealing in the fifteen-spined stickleback? Behavioral Ecology, 13, 188 192.
67. van Oppen MJH, Rico C, Deutsch JC, Turner GF, Hewitt GM (1997) Isolation and characterization of microsatellite loci in the cichlid fish Pseudotropheus zebra. Molecular Ecology, 6, 387 388.
68. Ota K, Kohda M (2006) Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika. Journal of Ethology, 24, 9 15.
69. Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environmental Biology of Fishes, 47, 345 352.
70. Queller DC (1997) Why do females care more than males? Proceedings of the Royal Society B: Biological Sciences, 264, 1555 1557.
71. Raymond M, Rousset F (1995) genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248.
72. Reichard M, Smith C, Jordan WC (2004) Genetic evidence reveals density-dependent mediated success of alternative mating behaviours in the European bitterling (Rhodeus sericeus). Molecular Ecology, 13, 1569 1578.
73. Rios-Cardenas O, Webster MS (2005) Paternity and paternal effort in the pumpkinseed sunfish. Behavioral Ecology, 16, 914 921.
74. Rossiter A (1991) Lunar spawning synchroneity in a freshwater fish. Naturwissenschaften, 78, 182 184.
75. Sato T, Hirose M, Taborsky M, Kimura S (2004) Size-dependent male alternative reproductive tactics in the shell-brooding cichlid fish Lamprologus callipterus in Lake Tanganyika. Ethology, 110, 49 62.
76. Sefc KM (2008) Variance in reproductive success and the opportunity for selection in a serially monogamous species: simulations of the mating system of Tropheus (Teleostei: Cichlidae). Hydrobiologia, in press.
77. Singer A, Kvarnemo C, Lindström K, Svensson 2006) Genetic mating patterns studied in pools with manipulated nest site availability in two populations of Pomatoschistus minutus. Journal of Evolutionary Biology, 19, 1641 1650.
78. Soucy S, Travis J (2003) Multiple paternity and population genetic structure in natural populations of the poeciliid fish, Heterandria formosa. Journal of Evolutionary Biology, 16, 1328 1336.
79. Steinfartz S, Stemshorn K, Kuesters D, Tautz D (2006) Patterns of multiple paternity within and between annual reproduction cycles of the fire salamander (Salamandra salamandra) under natural conditions. Journal of Zoology, 268, 1 8.
80. Sturmbauer C, Hahn C, Koblmüller S, Phiri H, Sinyinza D, Sefc KM (2008) Variation of territorial size and defense behavior in breeding pairs of the endemic Lake Tanganyika cichlid fish Variabilichromis moorii. Hydrobiologia, in press.
81. Sunobe T, Munehara H (2003) Mating system and kin relationship between adults and young in the shell-brooding cichlid fish Neolamprologus meeli in Lake Tanganyika. Journal of Ethology, 21, 87 92.
82. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior, 23, 1 100.
83. Taborsky M (2001) The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. Journal of Heredity, 92, 100 110.
84. Taborsky M (2008) Alternative reproductive tactics in fish. In : Alternative Reproductive Tactics (eds Oliveira R, Taborsky M, Brockmann J). Cambridge University Press, Cambridge, UK.
85. Taborsky M, Limberger D (1981) Helpers in fish. Behavioral Ecology and Sociobiology, 8, 143 145.
86. Tatarenkov A, Barreto F, Winkelman DL, Avise JC (2006) Genetic monogamy in the channel catfish, Ictalurus punctatus, a species with uniparental nest guarding. Copeia, 4, 735 741.
87. Taylor MI, Morley JI, Rico C, Balshine S (2003) Evidence of genetic monogamy and female-biased dispersal in the parental mouthbrooding cichlid Eretmodus cyanostictus from Lake Tanganyika. Molecular Ecology, 12, 3173 3177.
88. Trexler JC, Travis J, Dinep A (1997) Variation among populations of the sailfin molly in the rate of concurrent multiple paternity and its implications for mating-system evolution. Behavioral Ecology and Sociobiology, 40, 297 305.
89. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10, 506 513.
90. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics, 166, 1963 1979.
91. Wilson AB, Martin-Smith KM (2007) Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis). Molecular Ecology, 16, 2345 2352.
92. Wisenden BD (1999) Alloparental care in fishes. Reviews in Fish Biology and Fisheries, 9, 45 70.
93. Yamagishi S, Kohda M (1996) Is the cichlid fish Julidochromis marlieri polyandrous? Ichthyological Research, 43, 469 471.
94. Yanagisawa Y (1987) Social organization of a polygynous cichlid Lamprologus furcifer in Lake Tanganyika. Japanese Journal of Ichthyology, 34, 82 90.
95. Zardoya R, Vollmer DM, Craddock C, Streelman JT, Karl S, Meyer A (1996) Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proceedings of the Royal Society B: Biological Sciences, 263, 1589 1598.
96. Zbinden JA, Largiadér CR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Molecular Ecology, 16, 3703 3711.