Ovulation Order Mediates a Trade-Off between Pre-Hatching and Post-Hatching Viability in an Altricial Bird

Simultaneously dependent siblings often compete for parentally provided resources. This competition may lead to mortality, the probability of which may be a function, in part, of the individual offspring's production order. In birds, serial ovulation followed by hatching asynchrony of simultaneous dependents leads to differences in post-hatching survival that largely depend on ovulation (laying) order. This has led to the widespread assumption that early-laid eggs are of greater value and therefore should possess different maternally manipulated characteristics than later-laid eggs. However, this perspective ignores the potential effect of laying order on pre-hatching viability, an effect which some studies suggest should offset the effect of laying order on post-hatching viability. I examined the relationship between laying order and hatching and fledging probability in wild, free-living Lincoln's sparrows (Melospiza lincolnii). In broods with complete hatching success, first-laid and therefore first-hatched offspring had the highest probability of fledging, and fledging probability declined with increasing laying order. However, first-laid eggs were less likely than later-laid eggs to hatch. This effect of laying order on pre-hatching viability seemed to offset that on post-hatching viability, and, consistently, maternal investment in egg size varied little if at all with respect to laying order. These results suggest that ovulation order mediates a trade-off between pre-hatching and post-hatching viability and should encourage a re-evaluation of the solitary role post-embryonic survival often plays when researchers make assumptions about the value of propagules based on the order in which they are produced.

[1]  H. Schwabl,et al.  Sex-specific effects of yolk-androgens on growth of nestling American kestrels , 2008, Behavioral Ecology and Sociobiology.

[2]  A. J. Moore,et al.  Parents influence asymmetric sibling competition: experimental evidence with partially dependent young. , 2007, Ecology.

[3]  C. Wilson,et al.  The effects of exposure and microbes on hatchability of eggs in open‐cup and cavity nests , 2007 .

[4]  E. Virgós,et al.  Adaptive and Non-Adaptive Explanations for Hatching Failure in Eggs of the Red-Legged Partridge Alectoris rufa , 2007 .

[5]  P. Sharp,et al.  Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition , 2006, Biological reviews of the Cambridge Philosophical Society.

[6]  Sophia Rabe-Hesketh,et al.  Multilevel and Longitudinal Modeling Using Stata , 2005 .

[7]  Wesley M. Hochachka,et al.  Seasonal and latitudinal trends in clutch size : Thermal constraints during laying and incubation , 2005 .

[8]  S. Beissinger,et al.  Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. , 2005, Ecology letters.

[9]  S. Beissinger,et al.  Trans–shell infection by pathogenic micro–organisms reduces the shelf life of non–incubated bird's eggs: a constraint on the onset of incubation? , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  H. Goldstein,et al.  Partitioning variation in multilevel models , 2002 .

[11]  G. Hill,et al.  Sex-Biased Hatching Order and Adaptive Population Divergence in a Passerine Bird , 2002, Science.

[12]  E. Tkadlec,et al.  Analysis of brood sex ratios: implications of offspring clustering , 2001, Behavioral Ecology and Sociobiology.

[13]  N. Royle,et al.  Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? , 2001 .

[14]  J. Stevenson The evolution of sibling rivalry , 2000 .

[15]  H. Schwabl,et al.  Yolk androgens reduce offspring survival , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[16]  S. Beissinger,et al.  Egg viability as a constraint on hatching synchrony at high ambient temperatures , 1999 .

[17]  P. J. Cordero,et al.  Within-clutch patterns of egg viability and paternity in the House Sparrow , 1999 .

[18]  P. Monaghan,et al.  Experimental demonstration that offspring sex ratio varies with maternal condition. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  P. Monaghan,et al.  The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  G. Parker,et al.  Siblicide, family conflict and the evolutionary limits of selfishness , 1998, Animal Behaviour.

[21]  P. Burton,et al.  Extending the simple linear regression model to account for correlated responses: an introduction to generalized estimating equations and multi-level mixed modelling. , 1998, Statistics in medicine.

[22]  P. Monaghan,et al.  Why don't birds lay more eggs? , 1997, Trends in ecology & evolution.

[23]  D. Mock,et al.  A hormonal mechanism for parental favouritism , 1997, Nature.

[24]  C. Cicero Boggy meadows, livestock grazing, and interspecific interactions: influences on the insular distribution of montane Lincoln's Sparrows ( Melospiza lincolnii alticola ) , 1997 .

[25]  M. J. Stenning Hatching asynchrony, brood reduction and other rapidly reproducing hypotheses. , 1996, Trends in ecology & evolution.

[26]  S. Merino,et al.  Causes of Hatching Failure in the Pied Flycatcher , 1996 .

[27]  B. Pijanowski A Revision of Lack's Brood Reduction Hypothesis , 1992, The American Naturalist.

[28]  J. Veiga Hatching Asynchrony in the House Sparrow: A Test of the Egg-Viability Hypothesis , 1992, The American Naturalist.

[29]  R. Magrath HATCHING ASYNCHRONY IN ALTRICIAL BIRDS , 1990 .

[30]  T. Amundsen,et al.  Adaptive significance of asynchronous hatching in the shag: a test of the brood reduction hypothesis , 1988 .

[31]  T. Arnold,et al.  Egg Viability, Nest Predation, and the Adaptive Significance of Clutch Size in Prairie Ducks , 1987, The American Naturalist.

[32]  G. Bortolotti Influence of Sibling Competition on Nestling Sex Ratios of Sexually Dimorphic Birds , 1986, The American Naturalist.

[33]  D. Wilson,et al.  Avian Breeding Adaptations: Hatching Asynchrony, Brood Reduction, and Nest Failure , 1981, The Quarterly Review of Biology.

[34]  S. A. Barnett,et al.  The natural regulation of animal numbers , 1955 .

[35]  Alexis L. Romanoff,et al.  The avian egg , 1949 .

[36]  M. L. Morton The Mountain White-Crowned Sparrow: Migration and Reproduction at High Altitude , 2002 .

[37]  J. Amat,et al.  Intraclutch egg-size variation and offspring survival in the Kentish Plover Charadrius alexandrinus , 2001 .

[38]  S. Beissinger,et al.  Hatching Asynchrony and the Onset of Incubation in Birds, Revisited , 1995 .

[39]  R. Evans Terminal egg neglect in the american white pelican , 1990 .

[40]  D. F. Hoyt PRACTICAL METHODS OF ESTIMATING VOLUME AND FRESH WEIGHT OF BIRD EGGS , 1979 .

[41]  S. Baird,et al.  The birds of North America , 1974 .