Abstract
The relationship between offspring size and offspring number is crucial to life history evolution. To examine how these two life history variables are coupled and whether an altered balance between them will result in changes in maternal fitness, we manipulated clutch size of the Chinese cobra (Naja atra) by using the techniques of hormonal manipulation and follicle ablation. Females receiving exogenous follicle-stimulating hormone produced more but smaller eggs, and females undergoing follicle ablation produced fewer but larger eggs. Neither body size (body mass and snout-vent length) at hatching nor egg mass at oviposition had a role in determining hatchling survival and growth. Female hatchlings were more likely to die in early post-hatching days and grew more slowly than male hatchlings. Our data show that: (1) there is a nonlinear continuum of egg size-number trade-offs in N. atra within which there is a single inflexion where the rate at which egg size decreases with increasing clutch size, or clutch size increases with decreasing egg size, is maximized; (2) there is a fixed upper limit to egg size for a given-sized female, and the limit is not determined by her body volume; (3) egg size has no role in determining hatchling survival and growth; and (4) the extent to which females may enjoy reproductive benefits in a given reproductive episode depends on how well egg size and egg number are balanced.
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References
Agrawal AF, Brodie ED, Brown J (2001) Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292:1710–1712
Ballinger RE (1983) Life-history variations. In: Huey RB, Pianka ER, Tinkle TW (eds) Lizard ecology: studies of a model organism. Harvard University Press, Cambridge, pp 241–260
Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236
Boersma M (1997) Offspring size and parental fitness in Daphnia magna. Evol Ecol 11:439–450
Caley MJ, Schwarzkopf L, Shine R (2001) Does total reproductive effort evolve independently of offspring size? Evolution 55:1245–1248
Clutton-Brock T (1991) The evolution of parental care. Princeton University Press, Princeton
Congdon JD, Gibbons JW (1987) Morphological constraints on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci USA 84:4145–4147
Congdon JD, Nagle RD, Dunham AE, Beck CW, Kinney OM, Yeomans SR (1999) The relationship of body size to longevity of hatchling snapping turtles (Chelydra serpentina): an evaluation of the ‘bigger is better’ hypothesis. Oecologia 127:224–235
Dibattista JD, Feldheim KA, Gruber SH, Hendry AP (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. J Evol Biol 20:201–272
Downhower JF, Charnov EL (1998) A resource range invariance rule for optimal offspring size predicts patterns of variability in parental phenotypes. Proc Natl Acad Sci USA 95:6208–6211
Einum S, Flemming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567
Ferguson GW, Fox SF (1984) Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 38:342–349
Husak JF (2006) Does speed help you survive? A test with collared lizards of different ages. Funct Ecol 20:179–774
Janzen FJ, Tucker JK, Paukstis GL (2000a) Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. J Evol Biol 13:947–954
Janzen FJ, Tucker JK, Paukstis GL (2000b) Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81:2275–2280
Ji X, Diong CH (2006) Does follicle excision always result in enlargement of offspring size in lizards? J Comp Physiol B 176:521–525
Ji X, Du WG (2001) The effects of thermal and hydric conditions on incubating eggs and hatchling traits in the cobra, Naja naja atra. J Herpetol 35:186–194
Ji X, Du WG, Li H, Lin LH (2006) Experimentally reducing clutch size reveals a fixed upper limit to egg size in snakes: evidence from the king ratsnake (Elaphe carinata). Comp Biochem Physiol A 144:474–478
Ji X, Wang ZW (2005) Geographic variation in reproductive traits and trade-offs between size and number of eggs of the Chinese cobra, Naja atra. Biol J Linn Soc 85:27–40
Lin LH, Li H, An H, Ji X (2008) Do temperature fluctuations during incubation always play an important role in shaping the phenotype of hatchling reptiles? J Therm Biol 33:193–199
McGinley MA, Temme DH, Geber MA (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. Am Nat 130:370–398
Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, Oxford
Olsson M, Wapstra E, Olofsson C (2002) Offspring size-number strategies: experimental manipulation of offspring size in a viviparous lizard (Lacerta vivipara). Funct Ecol 16:135–140
Reznick DN, Bryga H (1987) Life-history evolution guppies (Poecilia reticulata). I. Phenotypic and genetic changes in an induced experiment. Evolution 41:1370–1385
Reznick DN, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357–359
Roff DA (2002) Life history evolution. Sinauer, Sunderland
Sargent RC, Taylor PD, Gross MR (1987) Parental care and the evolution of egg size in fishes. Am Nat 129:32–46
Sinervo B (1999) Mechanistic analysis of natural selection and a refinement of Lack’s and Williams’s principles. Am Nat 154:S26–S42
Sinervo B, Licht P (1991a) Hormonal and physiological control of clutch size, egg size and egg shape in side-blotched lizards (Uta stansburiana): constraints on the evolution of lizard life histories. J Exp Zool 257:252–264
Sinervo B, Licht P (1991b) Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252:1300–1302
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Warner DA, Andrews RM (2002) Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biol J Linn Soc 76:105–124
Warner DA, Shine R (2007) Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154:65–73
Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59
Winkler DW, Wallin K (1987) Offspring size and number: a life history model linking effort per offspring and total effort. Am Nat 129:708–720
Wüster W, Golay P, Warrell DA (1997) Synopsis of recent developments in venomous snake systematics. Toxicon 35:319–340
Acknowledgements
We thank Jian-Fang Gao, Hong-Liang Lu, Lai-Gao Luo, Yan-Yan Sun, Jing Yang and Ling Zhang for assistance in the laboratory, and F. Braña, R. B. Huey, R. Shine and D. W. Winkler for their insightful comments on an earlier draft of the paper. This work was carried out in compliance with the current laws of China, and was supported by grants from the Natural Science Foundation of China (NSFC30370229 and NSFC30770378) to X. J.
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Communicated by Raoul van Damme.
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Ji, X., Du, WG., Qu, YF. et al. Nonlinear continuum of egg size-number trade-offs in a snake: is egg-size variation fitness related?. Oecologia 159, 689–696 (2009). https://doi.org/10.1007/s00442-008-1252-2
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DOI: https://doi.org/10.1007/s00442-008-1252-2