Maternal effects increase within-family variation in offspring survival

American Naturalist

Volumn 174, Issue 5, 2009, Pages 685-695

  Reed, Wendy L ^a   Clark, Mark E ^a   Vleck, Carol M ^b  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Brood reduction; Egg size; Maternal investment; Offspring survival

Indexed keywords

BIRD; BROOD SIZE; EGG SIZE; FITNESS; LIFE HISTORY TRAIT; MATERNAL EFFECT; NATURAL SELECTION; PARENTAL INVESTMENT; PHENOTYPE; RESOURCE ALLOCATION; SURVIVAL;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIRD; CYTOLOGY; EVOLUTION; FEMALE; GENETIC SELECTION; HISTOLOGY; MATERNAL BEHAVIOR; NESTING; OOCYTE; PHYSIOLOGY;

ANIMALS; BIRDS; EVOLUTION; FEMALE; MATERNAL BEHAVIOR; MODELS, BIOLOGICAL; NESTING BEHAVIOR; OVUM; SELECTION, GENETIC;

FULICA AMERICANA;

EID: 72449208827     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/605962     Document Type: Article

References (87)

1. Agrawal, A. F., E. D. Brodie III, and M. J. Wade. 2001. On indirect genetic effects in structured populations. American Naturalist 158: 308-323.
2. Alatalo, R. V., L. Gustafson, and A. Lundberg. 1990. Phenotypic selection on heritable size traits: environmental variance and genetic response. American Naturalist 135:464-471.
3. Alisauskas, R. T. 1986. Variation in the composition of the eggs and chicks of American coots. Condor 88:84-90.
4. Amat, J. A., R. M. Fraga, and G. R. Arroyo. 2001. Intraclutch eggsize variation and offspring survival in the Kentish plover Charadrius alexandrinus. Ibis 143:17-23.
5. Amundsen, T., and J. N. Stokland. 1990. Egg size and parental quality influence nestling growth in the shag. Auk 107:410-413.
6. Amundsen T. Lorentsen S.-H. Tveraa T. Effects of egg size and parental quality on early nestling growth: an experiment with the Antarctic petrel Journal of Animal Ecology 1996 65 5 545-555. (Pubitemid 27048295)
7. Anderson, D. R., K. P. Burnham, and G. C. White. 1994. AIC model selection in overdispersed capture-recapture data. Ecology 75: 1780-1793.
8. Arnold, T. W., R. T. Alisauskas, and C. D. Ankney. 1991. Egg composition of American coots in relation to habitat, year, laying date, clutch size, and supplemental feeding. Auk 108:532-547.
9. Azevedo, R. B. R., V. French, and L. Partridge. 1997. Life-history consequences of egg size in Drosophila melanogaster. American Naturalist 150:250-282.
10. Badyaev, A. V., and K. P. Oh. 2008. Environmental induction and phenotypic retention of adaptive maternal effects. BMC Evolutionary Biology 8:3, doi:10.1186/1471-2148-8-3. http://www.biomedcentral.com/1471-2148/8/3.
11. Badyaev, A. V., D. Acevedo Seaman, K. J. Navara, G. E. Hill, and M. T. Mendonça. 2006. Evolution of sex-biased maternal effects in birds. III. Adjustment of ovulation order enables sex-specific allocation of hormones, carotenoids, and vitamins. Journal of Evolutionary Biology 19:1044-1057.
12. Badyaev, A. V., R. L. Young, G. E. Hill, and R. A. Duckworth. 2008. Evolution of sex-biased maternal effects in birds. IV. Intra-ovarian growth dynamics can link sex-determination and sex-specific acquisition of resources. Journal of Evolutionary Biology 21:449-460.
13. Bernardo, J. 1996a. Maternal effects in animal ecology. American Zoologist 36:83-105.
14. -. 1996b. The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. American Zoologist 36:216-236.
15. Bize P. Roulin A. Richner H. Covariation between egg size and rearing condition determines offspring quality: An experiment with the alpine swift Oecologia 2002 132 2 231-234 DOI 10.1007/s00442-002-0980-y. (Pubitemid 36064407)
16. Blomqvist D. Johansson O.C. Gotmark F. Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus Oecologia 1997 110 1 18-24 DOI 10.1007/s004420050128. (Pubitemid 27164692)
17. Bolton, M. 1991. Determinants of chick survival in the lesser blackbacked gull: relative contributions of egg size and parental quality. Journal of Animal Ecology 60:949-960.
18. Bonabeau E. Deneubourg J.-L. Theraulaz G. Within-brood competition and the optimal partitioning of parental investment American Naturalist 1998 152 3 419-427 DOI 10.1086/286179. (Pubitemid 28398078)
19. Brisbin, I. L., H. D. Pratt, and T. B. Mowbray. 2002. American coot (Fulica americana) and Hawaiian coot. (Fulica ahai). The Birds of North America, ed. A. Poole and F. Gill. No.697. Academy of Natural Sdences, Philadelphia; and American Ornithologists' Union, Washington, DC.
20. Burnham, K. P., and D. R. Anderson. 2002. Model selection and inference: a practical information-theoretic approach. Springer, New York.
21. Cheverud, J. M., and A. J. Moore. 1994. Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. Pages 67-100 in C. R. B. Boake, ed. Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago.
22. Christians, J. K. 2002. Avian egg size: variation within species and inflexibility within individuals. Biological Reviews of the Cambridge Philosophical Society 77:1-26.
23. Cormack, R. M. 1964. Estimates of survival from the sightings of marked animals. Biometrika 51:429-438.
24. Desrochers, B. A., and C. D. Ankney. 1986. Effects of brood size and age on the feeding behavior of adult and juvenile American coots (Fulica americana). Canadian Journal of Zoology 64:1400-1406.
25. Dziminski, M. A., and J. D. Roberts. 2006. Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana). Journal of Evolutionary Biology 19:144-155.
26. Einum, S., and I. A. Fleming. 2002. Does within-population variation in fish egg size reflect maternal influences on optimal values? American Naturalist 160:756-765.
27. Eising, C. M., and T. G. G. Groothuis. 2003. Yolk androgens and begging behavior in black-headed gull chicks: an experimental field study. Animal Behaviour 66:1027-1034.
28. Eising, C. M., C. Eikenaar, H. Schwabl, and T. G. G. Groothuis. 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proceedings of the Royal Society B: Biological Sciences 268:839-846.
29. Finkler, M. S., J. B. Van Orman, and P. R. Sutherland. 1998. Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird. Journal of Comparative Physiology B 168:17-24.
30. Forbes, S., and B. Glassey. 2000. Asymmetric sibling rivalry and nestling growth in red-winged blackbirds (Agelaius agelaius). Behavioral Ecology and Sodobiology 48:413-417.
31. Groothuis, T. G. G., W. Muller, N. von Engelhardt, C. Carere, and C. Eising. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 29:329-352.
32. Gullion, G. W. 1951. A marker for waterfowl. Journal of Wildlife Management 15:222-223.
33. Hendry, A. P., T. Day, and A. B. Cooper. 2001. Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. American Naturalist 157:387-407.
34. Hill, W. L. 1993. Importance of prenatal nutrition to the development of a precocial chick. Developmental Psychobiology 26:237-249.
35. Hipfner, J. M. 2000. The effect of egg size on post-hatching development in the razorbill: an experimental study. Journal of Avian Biology 31:112-118.
36. Hipfner, J. M., and A. J. Gaston. 1999. The relationship between egg size and posthatching development in the thick-billed murre. Ecology 80:1289-1297.
37. Hipfner, J. M., A. J. Gaston, and A. E. Storey. 2001. Food supply and the consequences of egg size in the thick-billed murre. Condor 103:240-247.
38. Hoyt, D. F. 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73-77.
39. Johnson, J. B., and K. S. Omland. 2004. Model selection in ecology and evolution. Trends in Ecology & Evolution 19:101-108.
40. Jolly, G. M. 1965. Explicit estimates from capture-recapture data with both death and immigration-stochastic model. Biometrika 52:225-247.
41. Krist, M., V. Remes, L. Uvirova, P. Nadvornik, and S. Bures. 2004. Egg size and offspring performance in the collared flycatcher (Ficedula albicollis): a within-clutch approach. Oecologia (Berlin) 140: 52-60.
42. Lack, D. 1968. Ecological adaptations for breeding in birds. Methuen, London.
43. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
44. Lebreton, J.-D., K. P. Burnham, J. Clobert, and D. R. Anderson. 1992. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62:67-118.
45. Lyon B.E. Conspecific brood parasitism as a flexible female reproductive tactic in American coots Animal Behaviour 1993 46 5 911-928 DOI 10.1006/anbe.1993.1273. (Pubitemid 24408900)
46. Lyon, B. E., J. M. Eadie, and L. D. Hamilton. 1994. Parental choice selects for ornamental plumage in American coot chicks. Nature 371:240-243.
47. Maddox, J. D., and P. J. Weatherhead. 2008. Egg size variation in birds with asynchronous hatching: is bigger really better? American Naturalist 171:358-365.
48. Magrath, R. D. 1992. Roles of egg mass and incubation pattern in establishment, of hatching hierarchies in the blackbird (Turdus merula). Auk 109:474-487.
49. McGraw, K. J., and D. R. Ardia. 2003. Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. American Naturalist. 162:704-712.
50. Mock, D. W., and G. A. Parker. 1997. The evolution of sibling rivalry. Oxford University Press, London.
51. Mousseau, T. A., and C. W. Fox, eds. 1998. Maternal effects as adaptations. Oxford University Press, London.
52. Muller W. Groothuis T.G.G. Kasprzik A. Dijkstra C. Alatalo R.V. Siitari H. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks Proceedings of the Royal Society B: Biological Sciences 2005 272 1575 1971-1977 DOI 10.1098/rspb.2005.3178. (Pubitemid 41414650)
53. Müller, W., C. M. Lessels, P. Korsten, and N. von Engelhardt. 2007. Manipulative signals in family conflict? on the function of maternal yolk hormones in birds. American Naturalist 169:E84-E96.
54. Naguib M. Gil D. Transgenerational effects on body size caused by early developmental stress in zebra finches Biology Letters 2005 1 1 95-97 DOI 10.1098/rsbl.2004.0277. (Pubitemid 41534580)
55. Navara, K. J., G. E. Hill, and M. T. Mendonça. 2005. Variable effects of yolk androgens on growth survival and immunity in eastern bluebird nestlings. Physiological and Biochemical Zoology 78:570-578.
56. -. 2006. Yolk testosterone stimulates growth and immunity in house finch chicks. Physiological and Biochemical Zoology 79:550-555.
57. Nichols, J. D. 2005. Modern open-population capture-recapture models. Pages 58-87 in S. C. Amstrup, T. L. McDonald, and B. F. J. Manly, eds. Handbook of capture-recapture analysis. Princeton University Press, Princeton, NJ.
58. Pelayo J.T. Clark R.G. Consequences of egg size for offspring survival: A cross-fostering experiment in Ruddy Ducks (Oxyura jamaicensis) Auk 2003 120 2 384-393. (Pubitemid 36774921)
59. Price T. Kirkpatrick M. Arnold S.J. Directional selection and the evolution of breeding date in birds Science 1988 240 4853 798-799. (Pubitemid 19319900)
60. Rasanen K. Kruuk L.E.B. Maternal effects and evolution at ecological time-scales Functional Ecology 2007 21 3 408-421 DOI 10.1111/j.1365-2435.2007. 01246.x. (Pubitemid 46805016)
61. Reed, W. L. 2000. Maternal effects in the American coot: consequences for offspring growth and survival. PhD diss. Iowa State University, Ames.
62. Reed, W. L., and C. M. Vleck. 2001. Functional significance of variation in egg-yolk androgens in the American coot. Oecologia (Berlin) 128:164-171.
63. Reed W.L. Turner A.M. Sotherland P.R. Consequences of egg-size variation in the red-winged blackbird Auk 1999 116 2 549-552. (Pubitemid 29207966)
64. Reid, W. V., and P. D. Boersma. 1990. Parental quality and selection on egg size in the Magellanic penguin. Evolution 44:1780-1786.
65. Ricklefs, R. E. 1984. Components of variance in measurements of nestling European starlings (Sturnus vulgaris) in southeastern Pennsylvania. Auk 101:319-333.
66. Ricklefs, R. E., and S. Peters. 1981. Parental components of variance in growth-rate and body size of nestling European starlings (Sturnus vulgaris) in eastern Pennsylvania. Auk 98:39-48.
67. Risch, T. S., and F. C. Rohwer. 2000. Effects of parental quality and egg size on growth and survival of herring gull chicks. Canadian Journal of Zoology 78:967-973.
68. Rollinson, N., and R. J. Brooks. 2008. Sources and significance of among-individual reproductive variation in a northern population of painted turtles (Chrysemys pieta). Copeia 2008:533-541.
69. Schwabl H. Environment modifies the testosterone levels of a female bird and its eggs Journal of Experimental Zoology 1996 276 2 157-163 DOI 10.1002/(SICI)1097-010X(19961001)276:2<157::AID-JEZ9>3.0.CO;2-N. (Pubitemid 27040114)
70. Seber, G. A. 1965. A note on the multiple recapture census. Biometrika 52:249-259.
71. Sinervo B. Licht P. Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards Science 1991 252 5010 1300-1302. (Pubitemid 21917042)
72. Slagsvold, T. J., J. Sandvik, G. Rofstad, Ö Lorentsen, and M. Husby. 1984. On the adaptive value of intraclutch egg-size variation in birds. Auk 101:685-697.
73. Smith, C. C., and S. D. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist. 108:499-506.
74. Smith, H. G., T. Ohlsson, and K. J. Wettermark. 1995. Adaptive significance of egg size in the European starling: experimental tests. Ecology 76:1-7.
75. Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford.
76. Stinchcombe, J. R., M. T. Rutter, D. S. Burdick, P. Tiffin, M. D. Rausher, and R. Mauricio. 2002. Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice. American Naturalist 160:511-523.
77. Styrsky, J. D., K. P. Eckerle, and C. F. Thompson. 1999. Fitnessrelated consequences of egg mass in nestling house wrens. Proceedings of the Royal Society B: Biological Sciences 266:1253-1258.
78. Valenzuela, N. 2001. Maternal effects on life history traits in the Amazonian giant river turtle Podocnemis expansa. Journal of Herpetology 35:368-378.
79. Van de Pol, M., T. Bakker, D. Saaltink, and S. Verhulst. 2006. Rearing conditions determine offspring survival independent of egg quality: a cross-foster experiment with oystercatchers Haematopus ostralegus. Ibis 148:203-210.
80. Wade, M. J. 1985. Soft, selection, hard selection, kin selection, and group selection. American Naturalist 125:61-73.
81. -. 1998. The evolutionary genetics of maternal effects. Pages 5-21 in T. A. Mousseau and C. W. Fox, eds. Maternal effects as adaptations. Oxford University Press, New York.
82. Wagner, E. C., and T. D. Williams. 2007. Experimental (antiestrogen-mediated) reduction in egg size negatively affects offspring growth and survival. Physiological and Biochemical Zoology 80:293-305.
83. White G.C. Burnham K.P. Program MARK: Survival estimation from populations of marked animals Bird Study 1999 46 SUPPL. S120-S139. (Pubitemid 30008152)
84. Williams, T. D. 1994. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biological Reviews 68:35-59.
85. Winemiller, K. O., and K. A. Rose. 1993. Why do most fish produce so many tiny offspring? American Naturalist 142:585-603.
86. Winkler, D. W., and K. Wallin. 1987. Offspring size and number: a life history model linking effort per offspring and total effort. American Naturalist 129:708-720.
87. Wolf, J. B., E. D. Brodie III, J. M. Cheverud, A. J. Moore, and M. J. Wade. 1998. Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution 13:64-69.