Conspicuous carotenoid-based pelvic spine ornament in three-spined stickleback populations-occurrence and inheritance

PeerJ

Volumn 2015, Issue 4, 2015, Pages

  Amundsen, C R ^a   Nordeide, J T ^a   Gjoen H M ^b   Larsen, B ^a   Egeland, E S ^a  

^a NORD UNIVERSITY   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Carotenoid; Female ornament; Gasterosteus aculeatus; Ornament; Pelvic spine; Signal; Stickleback

Indexed keywords

CAROTENOID;

ANIMAL EXPERIMENT; ARTICLE; FEMALE; GASTEROSTEUS ACULEATUS; GONAD; MALE; NONHUMAN; PREDICTION; PREVALENCE; PROGENY; REARING; RED PELVIC SPINE; SEASON; SPINE;

GASTEROSTEUS ACULEATUS; SCHISTOCEPHALUS SOLIDUS;

EID: 84926484933     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.872     Document Type: Article

References (75)

1. Amundsen T. 2000. Why are female birds ornamented? Trends in Ecology and Evolution 15:149-155 DOI 10.1016/S0169-5347(99)01800-5.
2. Amundsen T, Forsgren E. 2001. Male mate choice selects for female coloration in a fish. Proceedings of the National Academy of Sciences of the United States of America 6:13155-13160 DOI 10.1073/pnas.211439298.
3. Andersson M. 1994. Sexual selection. Princeton: Princeton University Press.
4. Bakker TCM. 1993. Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255-257 DOI 10.1038/363255a0.
5. Barber I. 2007. Host-parasite interactions of the three-spined sticklebacks. In: Östlund-Nilsson S, Mayer I, Huntingford FA, eds. Biology of the three-spined stickleback. Boca Raton: Taylor & Francis Group, 271-317.
6. Barber I, Arnott SA. 2000. Split-clutch IVF: a technique to examine indirect fitness consequences of mate preference in sticklebacks. Behaviour 137:1129-1140 DOI 10.1163/156853900502484.
7. Bell MA, Foster SA. 1994. The evolutionary biology of sticklebacks. Oxford: Oxford University Press.
8. Bigelow HB, SchroederWC. 1953. Fishes of the Gulf of Maine-first revision. Fisheries Bulletin of the Fish and Wildlife Service 53:307-312.
9. Bjerkeng B. 2008. Carotenoids in aquaculture: fish and crustaceans. In: Britton G, Liaaen-Jensen S, Pfander H, eds. Carotenoids-natural functions. Vol. 4. Basel: Birkhauser Verlag, 237-254.
10. Blount JD, Houston DC, Møller AP. 2000. Why egg yolk is yellow. Trends in Ecology and Evolution 15:47-49 DOI 10.1016/S0169-5347(99)01774-7.
11. Bonduriansky R. 2001. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews 76:305-339 DOI 10.1017/S1464793101005693.
12. Breder CM. 1960. Design for a fry trap. Zoologica 45:155-159.
13. Candolin U, Voigt HR. 2001. No effect of a parasite on reproduction in stickleback males: a laboratory artifact? Parasitology 122:457-464 DOI 10.1017/S0031182001007600.
14. Chenoweth SF, Doughty P, Kokko H. 2006. Can non-directional male mating preferences facilitate honest female ornamentation? Ecology Letters 9:179-184 DOI 10.1111/j.1461-0248.2005.00867.x.
15. Clutton-Brock T. 2009. Sexual selection in females. Animal Behaviour 77:3-11 DOI 10.1016/j.anbehav.2008.08.026.
16. Cronly-Dillon J, Sharma SC. 1968. Effect of season and sex on the photopic spectral sensivity of the three-spined stickleback. Journal of Experimental Biology 49:679-687.
17. Darwin C. 1871. The descent of man, and selection in relation to sex. London: Murrey.
18. Dupont-Nivet M, Vandeputte M, Chevassus B. 2002. Optimization of factorial mating designs for inference on heritability in fish species. Aquaculture 204:361-370 DOI 10.1016/S0044-8486(01)00839-0.
19. Elvingson P, Nilsson J. 1994. Phenotypic and genetic parameters of body and compositional traits in Arctic charr, Salvelinus alpinus (L.). Aquaculture and Fisheries Management 25:677-685 DOI 10.1111/j.1365-2109.1994.tb00732.x.
20. Evans SR, Sheldon BC. 2012. Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the Great tit. The American Naturalist 179:79-94 DOI 10.1086/663198.
21. Fitzpatrick S, Berglund A, Rosenqvist G. 1995. Ornaments or offspring: costs to reproductive success restrict sexual selection processes. Biological Journal of the Linnean Society 55:251-260 DOI 10.1111/j.1095-8312.1995.tb01063.x.
22. Folstad I, Hope AM, Karter A, Skorping A. 1994. Sexually selected color in male sticklebacks-a signal of both parasite exposure and parasite resistance. Oikos 69:511-515 DOI 10.2307/3545863.
23. Frischknecht M. 1993. The breeding colouration of male three-spined sticklebacks (Gasterosterus aculeatus) as an indicator of energy investment in vigour. Evolutionary Ecology 7:439-450 DOI 10.1007/BF01237640.
24. Funk DH, Tallamy DW. 2000. Courtship role reversal and deceptive signals in the long-tailed dance fly, Rhamphomyia longicauda. Animal Behaviour 59:411-421 DOI 10.1006/anbe.1999.1310.
25. Gladbach A, Gladbach DJ, Kempenaers B, Quillfeldt P. 2010. Female-specific colouration, carotenoids and reproductive investment in a dichromatic species, the upland goose Chloephaga picta leucoptera. Behavioral Ecology and Sociobiology 64:1779-1789 DOI 10.1007/s00265-010-0990-4.
26. Goodwin TW. 1984. The biochemistry of carotenoids, II. Animals. London: Chapman & Hall.
27. Grafen A, Hails R. 2002. Modern statistics for the life sciences. Oxford: Oxford University Press.
28. Grether GF, Hudon J, Endler JA. 2001. Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proceedings of the Royal Society B: Biological Sciences 268:1245-1253 DOI 10.1098/rspb.2001.1624.
29. Gross HP. 1978. Natural selection by predators on the defensive apparatus of the three-spined sticklebacks, Gasterosteus aculeatus L. Canadian Journal of Zoology 56:398-413 DOI 10.1139/z78-058.
30. Hadfield JD, Burgess MD, Lord A, Phillimore AB, Clegg SM, Owens IPF. 2006. Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird. Proceedings of the Royal Society B-Biological Sciences 273:1347-1353 DOI 10.1098/rspb.2005.3459.
31. Hadfield JD, Owens IPF. 2006. Strong environmental determination of a carotenoid-based plumage trait is not mediated by carotenoid availability. Journal of Evolutionary Biology 19:1104-1114 DOI 10.1111/j.1420-9101.2006.01095.x.
32. Hagen DW, Gilbertson LG. 1972. Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest, America. Evolution 26:32-51 DOI 10.2307/2406981.
33. Hill GE. 1993a. Geographic variation in the carotenoid plumage pigmentation of male House Finches (Carpodacus mexicanus). Biological Journal of the Linnean Society 49:63-86 DOI 10.1111/j.1095-8312.1993.tb00685.x.
34. Hill GE. 1993b. The proximate basis of inter-population and intra-population variation in female plumage coloration in the House Finch. Canadian Journal of Zoology-Revue Canadienne De Zoologie 71:619-627 DOI 10.1139/z93-084.
35. Hodgson A, Black AR, Hull R. 2013. Sensory exploitation and indicator models may explain red pelvic spines in the brook stickleback, Culaea inconstans. Evolutionary Ecology Research 15:199-211.
36. Kempthorne O, Tandon OB. 1953. The estimation of heritability by regression of offspring on parent. Biometrics 9:90-100 DOI 10.2307/3001635.
37. Klepaker TO, Østbye K. 2008. Pelvic anti-predator armour reduction in Norwegian populations of the threespine stickleback: a rare phenomenon with adaptive implications? Journal of Zoology 276:81-88 DOI 10.1111/j.1469-7998.2008.00471.x.
38. Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J. 2007. The evolution of mutual ornamentation. Animal Behaviour 74:657-677 DOI 10.1016/j.anbehav.2006.12.027.
39. Lande R. 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292-305 DOI 10.2307/2407393.
40. LeBas NR, Hockham LR, Ritchie MG. 2003. Nonlinear and correlational sexual selection on 'honest' female ornamentation. Proceedings of the Royal Society B: Biological Sciences 270:2159-2165 DOI 10.1098/rspb.2003.2482.
41. Lythgoe JN. 1979. The ecology of vision. Oxford: Clarendon Press. Massaro M, Davis MS, Darby JT. 2003. Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguins (Megadyptes antipodes). Behavioral Ecology and Sociobiology 55:169-175 DOI 10.1007/s00265-003-0683-3.
42. McKinnon JS, Demayo RF, Granquist R, Weggel L. 2000. Female red throat coloration in two populations of threespine stickleback. Behaviour 137:947-963 DOI 10.1163/156853900502556.
43. McLennan DA. 1994. Changes in female colour across the ovulatory cycle in the brook stickleback, Culaea inconstans (Kirtland). Canadian Journal of Zoology 72:144-153 DOI 10.1139/z94-018.
44. McLennan DA. 1995. Male mate choice based upon female nuptial coloration in the brook stickleback, Culaea inconstans (Kirtland). Animal Behaviour 50:213-221 DOI 10.1006/anbe.1995.0233.
45. Milinski M. 2014. The past and the future of Behavioral Ecology. Behavioral Ecology 25:680-684 DOI 10.1093/beheco/aru079.
46. Milinski M, Bakker TCM. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330-333 DOI 10.1038/344330a0.
47. Moodie GEE. 1972. Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28:115-167 DOI 10.1038/hdy.1972.21.
48. Muller W, Vergauwen J, Eens M, Blount J. 2012. Environmental effects shape the maternal transfer of carotenoids and vitamin E to the yolk. Frontiers in Zoology 9:17 DOI 10.1186/1742-9994-9-17.
49. Neff BD, Garner SR, Heath JW, Heath D. 2008. The MHC and non-random mating in a captive population of Chinook salmon. Heredity 101:175-185 DOI 10.1038/hdy.2008.43.
50. Nordeide JT. 2002. Do male sticklebacks prefer females with red ornamentation? Canadian Journal of Zoology 80:1344-1349 DOI 10.1139/z02-116.
51. Nordeide JT, Kekäläinen J, Janhunen M, Kortet R. 2013. Female ornaments revisited-are they correlated with offspring quality? Journal of Animal Ecology 82:26-38 DOI 10.1111/1365-2656.12021.
52. Nordeide JT, Mohus A, Nicolaisen O, Volden R, Egeland ES. 2008. Offspring or ornaments? Is carotenoid-based ornamentation in female Arctic charr, Salvelinus alpinus (L.), condition-dependent and traded off against offspring? Ecology of Freshwater Fish 17:328-339 DOI 10.1111/j.1600-0633.2007.00286.x.
53. Nordeide JT, Rudolfsen G, Egeland ES. 2006. Ornaments or offspring? Female sticklebacks (Gasterosteus aculeatus L.) trade off carotenoids between spines and eggs. Journal of Evolutionary Biology 19:431-439 DOI 10.1111/j.1420-9101.2005.01018.x.
54. Ostlund-Nilsson S, Mayer I, Huntingford FA. 2007. Biology of the three-spined stickleback. Boca Raton: CRC Press, Taylor & Francis Group.
55. Pagani-Núñez E, Uribe F, Hernández-Gómez S, Muñoz G, Senar JC. 2014. Habitat structure and prey composition generate contrasting effects on carotenoid-based coloration of great tit Parus major nestlings. Biological Journal of the Linnean Society 113:547-555 DOI 10.1111/bij.12352.
56. Pethon P. 1985. Aschehougs store fiskebok. Oslo: H. Aschehoug & Co A/S.
57. Price DK. 1996. Sexual selection, selection load and quantitative genetics of zebra finch bill colour. Proceedings of the Royal Society of London Series B-Biological Sciences 263:217-221 DOI 10.1098/rspb.1996.0034.
58. Rick I, Bakker T. 2008a. UV wavelengths make female three-spined sticklebacks (Gasterosteus aculeatus) more attractive for males. Behavioral Ecology and Sociobiology 62:439-445 DOI 10.1007/s00265-007-0471-6.
59. Rick IP, Bakker TCM. 2008b. Color signaling in conspicuous red sticklebacks: do ultraviolet signals surpass others? BMC Evolutionary Biology 8:189 DOI 10.1186/1471-2148-8-189.
60. Rowe MP, Baube CL, Loew ER, Phillips JB. 2004. Optimal mechanisms for finding and selecting mates: how threespine stickleback (Gasterosteus aculeatus) should encode male throat colors. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 190:241-256 DOI 10.1007/s00359-004-0493-8.
61. Rowland WJ. 1994. Proximate determinants of stickleback behaviour: an evolutionary perspective. In: Foster SA, Bell MA, eds. The evolutionary biology of the threespine stickleback. Oxford: Oxford University Press, 297-344.
62. Rowland WJ, Baube CL, Horan TT. 1991. Signalling of sexual receptivity by pigmentation pattern in female sticklebacks. Animal Behaviour 42:243-249 DOI 10.1016/S0003-3472(05)80555-X.
63. Rudolfsen G, Figenschou L, Folstad I, Nordeide JT, Søreng E. 2005. Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua). Journal of Evolutionary Biology 18:172-179 DOI 10.1111/j.1420-9101.2004.00778.x.
64. Simmons LW. 2014. 25 years of Behavioral Ecology. Behavioral Ecology 25:1-3 DOI 10.1093/beheco/art108.
65. Skarstein F, Folstad I. 1996. Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76:359-367 DOI 10.2307/3546208
66. Skarstein F, Folstad I, Rønning HP. 2005. Spawning colouration, parasites and habitat selection in Salvelinus alpinus: initiating speciation by sexual selection? Jounal of Fish Biology 67:969-980 DOI 10.1111/j.0022-1112.2005.00796.x.
67. ter Pelkwijk JJ, Tinbergen N. 1937. Eine reizbiologische Analyse einige Verhaltsweisen von Gasterostus aculeatus L. Zeitschrift für Tierpsychologie 1:193-200 DOI 10.1111/j.1439-0310.1937.tb01422.x.
68. Tinbergen N. 1948. Social releasers and the experimental method required for their study. Wilson Bulletin 60:6-51.
69. Villafuerte R, Negro JJ. 1998. Digital imaging for colour measurement in ecological research. Ecology Letters 1:151-154 DOI 10.1046/j.1461-0248.1998.00034.x.
70. von Hippel FA. 1999. Black male bellies and red female throats: color changes with breeding status in a threespine stickleback. Environmental Biology of Fishes 55:237-244 DOI 10.1023/A:1007572620424.
71. Withler RE. 1986. Genetic variation in carotenoid pigment deposition in the red-fleshed and white fleshed chinook salmon (Oncorhynchus tshawytscha) of Quesnel River, British Columbia. Canadian Journal of Genetics and Cytology 28:587-594 DOI 10.1139/g86-086.
72. Wootton RJ. 1976. The biology of sticklebacks. London: Academic Press.
73. Wootton RJ. 1984. A functional biology of sticklebacks. London: Croom Helm.
74. Yong L, Guo R, Wright DS, Mears SA, Pierotti M, McKinnon JS. 2013. Correlates of red throat coloration in female stickleback and their potential evolutionary significance. Evolutionary Ecology Research 15:453-472.
75. Zahavi A. 1975. Mate selection-a selection for a handicap. Journal of Theoretical Biology 53:205-214 DOI 10.1016/0022-5193(75)90111-3.