Advertisement

Oecologia

, Volume 154, Issue 1, pp 65–73 | Cite as

Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size

  • Daniel A. Warner
  • Richard Shine
Population Ecology

Abstract

To understand how selection shapes life-history traits, we need information on the manner in which offspring phenotypes influence fitness. Life-history allocation models typically assume that “bigger offspring are better”, but field data paint a more complex picture: larger offspring size sometimes enhances fitness, and sometimes not. Additionally, higher survival and faster growth of larger offspring might be due to indirect maternal effects (e.g., mothers allocate hormones or nutrients differently to different-sized eggs), and not to offspring size per se. Alternative factors, such as seasonal timing of hatching, may be more important. We examined these issues using 419 eggs from captive jacky dragon lizards (Amphibolurus muricatus). The mothers were maintained under standardized conditions to minimize variance in thermal and nutritional history, and the eggs were incubated under controlled conditions to minimize variance in offspring phenotypes due to incubation temperature and moisture. We reduced the size of half the eggs (and, thus, the size of the resultant hatchlings) from each clutch by yolk extraction. The hatchlings were marked and released at a field site over a 3-month period, with regular recapture surveys to measure growth and survival under natural conditions. Growth rates and survival were strongly enhanced by early-season hatching, but were not affected by hatchling body size.

Keywords

Amphibolurus muricatus Body size Jacky dragon Growth rate Offspring survival 

Notes

Acknowledgments

We thank T. Child, T. Schwartz, J. Thomas, and C. Warner for assistance in the field. DAW was supported by and International Postgraduate Research Scholarship and International Postgraduate Award. This project was supported by grants from the Australian Society of Herpetologists (to DAW) and the Australian Research Council (to RS). This project was approved by the University of Sydney Animal Care and Ethics Committee (proposal no L04/12-2004/1/4018), and the New South Wales National Parks and Wildlife Service (license no. S10658).

References

  1. Andrews RM, Mathies T, Warner DA (2000) Effect of incubation temperature on morphology, growth, and survival of juvenile Sceloporus undulatus. Herpetol Monogr 14:420–431CrossRefGoogle Scholar
  2. Brown GP, Shine R (2006) Why do most tropical animals reproduce seasonally? Testing hypotheses on an Australian snake. Ecology 87:133–143CrossRefPubMedGoogle Scholar
  3. Cogger HG (2000) Reptiles and amphibians of Australia. New Holland Publ, SydneyGoogle Scholar
  4. 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 121:224–235CrossRefPubMedGoogle Scholar
  5. Daan S, Dijkstra C, Weissing FJ (1996) An evolutionary explanation for seasonal trends in avian sex ratios. Behav Ecol 7:426–430CrossRefGoogle Scholar
  6. 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 20:201–212CrossRefPubMedGoogle Scholar
  7. Einum S, Flemming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567CrossRefPubMedGoogle Scholar
  8. Gil D, Ninni P, Lacroix A, DeLope R, Tirard C, Marzal A, Møller AP (2006) Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses. J Evol Biol 19:123–131CrossRefPubMedGoogle Scholar
  9. Ferguson GW, Bohlen CH (1978) Demographic analysis: a tool for the study of natural selection of behavioral traits. In: Greenberg N, Maclean PD (eds) Behavior and neurology of lizards. DHEW Publication No. (ADM) 77–491, Washington D.C., pp 227–243Google Scholar
  10. Ferguson GW, Fox SF (1984) Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 38:342–349CrossRefGoogle Scholar
  11. Forsman A (1993) Survival in relation to body size and growth rate in the adder, Vipera berus. J Anim Ecol 62:647–655CrossRefGoogle Scholar
  12. Gerwien RW, John-Alder HB (1992) Growth and behavior of thyroid deficient lizards (Sceloporus undulatus). Gen Comp Endocrinol 87:312–324CrossRefPubMedGoogle Scholar
  13. Harlow PS (1996) A harmless technique for sexing hatchling lizards. Herpetol Rev 27:71–72Google Scholar
  14. Harlow PS, Taylor JE (2000) The reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Aust Ecol 25:640–652CrossRefGoogle Scholar
  15. Heath DD, Blouw DM (1998) Are maternal effects in fish adaptive or merely physiological side effects? In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 178–201Google Scholar
  16. Husak JF (2006) Does speed help you survive? A test with collard lizards of different ages. Funct Ecol 20:174–179CrossRefGoogle Scholar
  17. Husak JF, Fox SF, Lovern MB, Van Den Bussche RA (2006) Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 60:2122–2130CrossRefPubMedGoogle Scholar
  18. Janzen FJ (1993) An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74:332–341CrossRefGoogle Scholar
  19. Janzen FJ (1995) Experimental evidence for the evolutionary significance of temperature-dependent sex determination. Evolution 49:864–873CrossRefGoogle Scholar
  20. Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571CrossRefGoogle Scholar
  21. 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 13:947–954CrossRefGoogle Scholar
  22. Janzen FJ, Tucker JK, Paukstis GL (2000b) Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81:2290–2304CrossRefGoogle Scholar
  23. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  24. Langkilde T, Shine R (2005) Different optimal offspring sizes for sons versus daughters may favour the evolution of temperature-dependent sex determination in viviparous lizards. Evolution 59:2275–2280CrossRefPubMedGoogle Scholar
  25. Lorenzon P, Clobert J, Oppliger A, John-Alder H (1999) Effect of water constraint on growth rate, activity and body temperature of yearling common lizards (Lacerta vivipara). Oecologia 118:423–430CrossRefPubMedGoogle Scholar
  26. Miles DB (2004) The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evol Ecol Res 6:63–75Google Scholar
  27. Myers JH (1981) Interactions between western tent caterpillars and wild rose: a test of some general plant herbivore hypotheses. J Anim Ecol 50:11–25CrossRefGoogle Scholar
  28. Olsson M, Madsen T (2001) Between-year variation in determinants of offspring survival in the sand lizard, Lacerta agilis. Funct Ecol 15:443–450CrossRefGoogle Scholar
  29. Olsson M, Shine R (1997) The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better. J Evol Biol 10:369–381CrossRefGoogle Scholar
  30. Olsson M, Shine R (2002) Growth to death in lizards. Evolution 56:1867–1870CrossRefPubMedGoogle Scholar
  31. Packard GC, Packard MJ (1988) The physiological ecology of reptile eggs and embryos. In: Gans C, Huey RB (eds) Biology of the reptilia, vol 16. Alan R. Liss, New York, pp 523–605Google Scholar
  32. Perrins CM (1967) Survival of young manx shearwaters Puffinus puffinus in relation to their presumed dates of hatching. Ibis 108:132–135CrossRefGoogle Scholar
  33. Qualls FJ, Shine R (2000) Post-hatching environment contributes greatly to phenotypic variation between two populations of the Australian garden skink, Lampropholis guichenoti. Biol J Linn Soc 71:315–341CrossRefGoogle Scholar
  34. Radder RS, Shanbhag BA (2003) Interrelationships among reproductive traits of female lizard, Sitana ponticeriana (Cuvier). Curr Sci 85:89–91Google Scholar
  35. Ryan TJ, Plague GR (2004) Hatching asynchrony, survival, and the fitness of alternative adult morphs in Ambystona talpoideum. Oecologia 140:46–51CrossRefPubMedGoogle Scholar
  36. SAS Institute Inc (1997) SAS/STAT user’s guide. Statistical Analysis Systems Institute, Cary, N.C.Google Scholar
  37. Schluter D (1988) Estimating the form of natural selection on a quantitative trait. Evolution 42:849–861CrossRefGoogle Scholar
  38. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  39. Shanbhag BA, Radder RS, Saidapur SK (2000) Maternal size determines clutch mass, whereas breeding timing influences clutch and egg sizes in the tropical lizard, Calotes versicolor (Agamidae). Copeia 2000:1062–1067CrossRefGoogle Scholar
  40. Sinervo B (1998) Adaptation of maternal effects in the wild: path analysis of natural variation and experimental tests of causation. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 288–306Google Scholar
  41. Sinervo B, Doughty P, Huey RB, Zamudio K (1992) Allometric engineering: a causal analysis of natural selection on offspring size. Science 258:1927–1930CrossRefPubMedGoogle Scholar
  42. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506CrossRefGoogle Scholar
  43. Sorci G, Clobert J (1999) Natural selection on hatchling body size and mass in two environments in the common lizard (Lacerta vivipara). Evol Ecol Res 1:303–316Google Scholar
  44. Tinkle DW (1967) The life and demography of the side-blotched lizard, Uta stansburiana. Miscellaneous publications (no. 132). Museum of Zoology, University of Michigan, Ann ArborGoogle Scholar
  45. Warner DA, Andrews RM (2002) Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biol J Linn Soc 76:105–124CrossRefGoogle Scholar
  46. Warner DA, Shine R (2005) The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard. Evolution 59:2209–2221CrossRefPubMedGoogle Scholar
  47. Warner DA, Lovern MB, Shine R (2007) Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination. Proc R Soc Lond B 274:883–890CrossRefGoogle Scholar
  48. Webb JK, Shine R, Christian KA (2006) The adaptive significance of reptilian viviparity in the tropics: testing the maternal manipulation hypothesis. Evolution 60:115–122PubMedGoogle Scholar
  49. Wilbur HM, Morin PJ (1988) Life history evolution in turtles. In: Gans C, Huey RB (eds) Biology of the reptilia, vol 16. Alan R Liss, New York, pp 387–439Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of SydneySydneyAustralia
  2. 2.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA

Personalised recommendations