Egg environments have large effects on embryonic development, but have minimal consequences for hatchling phenotypes in an invasive lizard

Biological Journal of the Linnean Society

Volumn 105, Issue 1, 2012, Pages 25-41

  Warner, Daniel A ^a   Moody, Melissa A ^a,b   Telemeco, Rory S ^a   Kolbe, Jason J ^c  

^a IOWA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Body size; Developmental plasticity; Egg incubation; Egg size; Incubation moisture; Incubation temperature; Limb length; Residual yolk

Indexed keywords

ADAPTATION; BODY SIZE; COLONIZATION; EGG SIZE; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL FACTOR; FITNESS; FUNCTIONAL MORPHOLOGY; HATCHING; INCUBATION; INVASIVE SPECIES; LIZARD; METABOLISM; MOISTURE; PHENOTYPE; PHENOTYPIC PLASTICITY; TAXONOMY; TEMPERATURE EFFECT; TOLERANCE; WATER USE;

EID: 83155173322     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2011.01778.x     Document Type: Article

References (91)

1. Andrews RM. 1982. Spatial variation in egg mortality of the lizard Anolis limifrons. Herpetologica 38: 165-171.
2. Andrews RM. 2004. Patterns of embryonic development. In: Deeming DC, ed. Reptilian incubation: environment, evolution and behaviour. Nottingham: Nottingham University Press, 75-102.
3. Andrews RM, Mathies T, Warner DA. 2000. Effect of incubation temperature on morphology, growth, and survival of juvenile Sceloporus undulatus. Herpetological Monographs 14: 420-431.
4. Andrews RM, Sexton OJ. 1981. Water relations of the eggs of Anolis auratus and Anolis limifrons. Ecology 62: 556-562.
5. Angilletta MJ Jr. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford: Oxford University Press.
6. Ashmore GM, Janzen FJ. 2003. Phenotypic variation in smooth softshell turtles (Apalone mutica) from eggs incubated in constant versus fluctuating temperatures. Oecologia 134: 182-188.
7. Beldade P, Mateus ARA, Keller RA. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology 20: 1347-1363.
8. Belinsky A, Ackerman RA, Dmi'el R, Ar A. 2004. Water in reptilian eggs and hatchlings. In: Deeming DC, ed. Reptilian incubation: environment, evolution and behaviour. Nottingham: Nottingham University Press, 125-141.
9. Braña F, Ji X. 2000. Influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcis muralis). Journal of Experimental Zoology 286: 422-433.
10. Brown GP, Shine R. 2005. Do changing moisture levels during incubation influence phenotypic traits of hatchling snakes (Tropidonophis mairii, Colubridae)? Physiological and Biochemical Zoology 78: 524-530.
11. Calsbeek R, Irschick DJ. 2007. The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61: 2493-2503.
12. Chandler CH. 2010. Cryptic intraspecific variation in sex determination in Caenorhabditis elegans revealed by mutations. Heredity 105: 473-482.
13. Christian KA, Lawrence WT, Snell HL. 1991. Effect of soil moisture on yolk and fat distribution in hatchling lizards from natural nests. Comparative Biochemistry and Physiology 99A: 13-19.
14. Cleasby IR, Nakagawa A, Gillespie DOS, Burke T. 2010. The influence of sex and body size on nestling survival and recruitment in the house sparrow. Biological Journal of the Linnean Society 101: 680-688.
15. Deeming DC. 2004. Reptilian incubation: environment, evolution and behaviour. Nottingham: Nottingham University Press.
16. DeWitt TJ, Scheiner SM. 2004. Phenotypic plasticity: functional and conceptual approaches. Oxford: Oxford University Press.
17. Downes SJ, Shine R. 1999. Do incubation-induced changes in a lizard's phenotype influence its vulnerability to predators? Oecologia 120: 9-18.
18. Du W-G, Ji X. 2006. Effects of constant and fluctuating temperatures on egg survival and hatchling traits in the northern grass lizard (Takydromus septentrionalis, Lacertidae). Journal of Experimental Zoology 305A: 47-54.
19. Du W-G, Ye H, Zhao B, Warner DA, Shine R. 2010. Thermal acclimation of heart rates in reptilian embryos. PLoS One 5: 1-7.
20. Elphick MJ, Shine R. 1998. Long-term effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae). Biological Journal of the Linnean Society 63: 429-447.
21. Engqvist L. 2005. The mistreatment of covariate interactions in linear model analysis of behavioural and evolutionary ecology studies. Animal Behaviour 70: 967-971.
22. Flatt T, Shine R, Borges-Landaez PA, Downes SJ. 2001. Phenotypic variation in an oviparous montane lizard (Bassiana duperreyi): the effects of thermal and hydric incubation environments. Biological Journal of the Linnean Society 74: 339-350.
23. Ghalambor CK, McKay JK, Carroll SP, Reznick DN. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21: 394-407.
24. Gilbert SF, Epel D. 2008. Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sunderland: Sinauer.
25. Goodman RM. 2008. Latent effects of egg incubation temperature on growth in the lizard Anolis carolinensis. Journal of Experimental Zoology 309A: 525-533.
26. Goodman RM, Walguarnery JW. 2007. Incubation temperature modifies neonatal thermoregulation in the lizard Anolis carolinensis. Journal of Experimental Zoology 307A: 439-448.
27. Gurganus MC, Fry JD, Nuzhdin SV, Pasyukova EG, Lyman RF, Mackay TFC. 1998. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. Genetics 149: 1883-1898.
28. Gutzke WHN, Crews D. 1988. Embryonic temperature determines adult sexuality in a reptile. Nature 332: 832-834.
29. Janzen FJ. 1993. An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74: 332-341.
30. Janzen FJ, Packard GC, Packard MJ, Boardman TJ, ZumBrunnen JR. 1990. Mobilization of lipid and protein by embryonic snapping turtles in wet and dry environments. Journal of Experimental Zoology 255: 155-162.
31. Janzen FJ, Tucker JK, Paukstis GL. 2000. Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81: 2290-2304.
32. Ji X, Braña F. 1999. The influence of thermal and hydric environments on embryonic use of energy and nutrients, and hatchling traits, in the wall lizards (Podarcis muralis). Comparative Biochemistry and Physiology A 124: 205-213.
33. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB. 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177-181.
34. Kolbe JJ, Janzen FJ. 2002. Experimental analysis of an early life-history stage: water loss and migrating hatchling turtles. Copeia 2002: 220-226.
35. Kolbe JJ, Losos JB. 2005. Hind-limb length plasticity in Anolis carolinensis. Journal of Herpetology 39: 674-678.
36. Laurie WA, Brown D. 1990. Population biology of marine iguanas (Amblyrhyncus cristatus). II. Changes in annual survival rates and the effects of size, sex, age and fecundity in a population crash. Journal of Animal Ecology 59: 529-544.
37. Lee JC, Clayton D, Eisenstein S, Perez I. 1989. The reproductive cycle of Anolis sagrei in southern Florida. Copeia 1989: 930-937.
38. Losos JB. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Berkeley, CA: University of California Press.
39. Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N, Taylor P, Ettling J. 2000. Evolutionary implication of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54: 301-305.
40. Losos JB, Schoener TW, Spiller DA. 2003. Effect of immersion in seawater on egg survival in the lizard Anolis sagrei. Oecologia 137: 360-362.
41. Marguis O, Massot M, Le Galliard JF. 2008. Intergenerational effects of climate generate cohort variation in lizard reproductive performance. Ecology 89: 2575-2583.
42. Miller K, Packard GC. 1992. The influence of substrate water potential during incubation on the metabolism of embryonic snapping turtles (Chelydra serpentina). Physiological Zoology 65: 172-187.
43. Miller K, Packard GC, Packard MJ. 1987. Hydric conditions during incubation influence locomotor performance of hatchling snapping turtles. Journal of Experimental Biology 127: 401-412.
44. Morris KA, Packard GC, Boardman TJ, Paukstis GL, Packard MJ. 1983. Effect of the hydric environment on growth of embryonic snapping turtles (Chelydra serpentina). Herpetologica 39: 272-285.
45. Nagle RD, Burke VJ, Congdon JD. 1998. Egg components and hatchling lipid reserves: parental investment in kinosternid turtles from the southeastern United States. Comparative Biochemistry and Physiology B 120: 145-152.
46. Olsson M, Shine R. 1997. The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better. Journal of Evolutionary Biology 10: 369-381.
47. Overall KL. 1994. Lizard egg environments. In: Vitt LJ, Pianka ER, eds. Lizard ecology: historical and experimental perspectives. Princeton, NJ: Princeton University Press, 51-72.
48. Packard GC, Packard MJ. 1988. The physiological ecology of reptilian eggs and embryos. In: Gans C, Huey RB, eds. Biology of the Reptilia. 16. New York: Alan R. Liss, 523-605.
49. Packard GC, Packard MJ, Miller K, Boardman TJ. 1987. Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos. Ecology 68: 983-993.
50. Packard GC, Packard MJ, Miller K, Boardman TJ. 1988. Effects of temperature and moisture during incubation on carcass composition of hatchling snapping turtles (Chelydra serpentina). Journal of Comparative Physiology B 158: 117-125.
51. Packard GC, Paukstis GL, Boardman TJ, Gutzke WHN. 1985. Daily and seasonal variation in hydric conditions and temperature inside nests of common snapping turtles (Chelydra serpentina). Canadian Journal of Zoology 63: 2422-2429.
52. Packard MJ, Packard GC, Boardman TJ. 1980. Water balance of the eggs of a desert lizard (Callisaurus draconoides). Canadian Journal of Zoology 58: 2051-2058.
53. Perez KO, Munch SB. 2010. Extreme selection on size in the early lives of fish. Evolution 64: 2450-2457.
54. Perrins CM. 1967. Survival of young manx shearwaters Puffinus puffinus in relation to their presumed dates of hatching. Ibis 108: 132-135.
55. Phillips JA, Garel A, Packard GC, Packard MJ. 1990. Influence of moisture and temperature on eggs and embryos of green iguanas (Iguana iguana). Herpetologica 46: 238-245.
56. Phillips JA, Packard GC. 1994. Influence of temperature and moisture on eggs and embryos of the white-throated savanna monitor Varanus albigularis: implications for conservation. Biological Conservation 69: 131-136.
57. Prosser C, Hudson S, Thompson MB. 2006. Effects of urbanization on behavior, performance, and morphology of the garden skink, Lampropholis guichenoti. Journal of Herpetology 40: 151-159.
58. Radder RS, Shanbhag BA, Saidapur SK. 2004. Yolk partitioning in embryos of the lizard Calotes vericolor: maximize body size or use energy for later use? Journal of Experimental Zoology 301A: 783-785.
59. Radder RS, Warner DA, Cuervo JJ, Shine R. 2007. The functional significance of residual yolk in hatchling lizards Amphibolurus muricatus (Agamidae). Functional Ecology 21: 302-309.
60. Refsnider JM, Janzen FJ. 2010. Puttings eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annual Review of Ecology, Evolution, and Systematics 41: 39-57.
61. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
62. Robbins TR, Warner DA. 2010. Fluctuations in the incubation moisture environment affect growth but not survival of hatchling lizards. Biological Journal of the Linnean Society 100: 89-102.
63. Sanger TJ, Hime PM, Johnson MA, Diani J, Losos JB. 2008a. Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herpetological Review 39: 58-63.
64. Sanger TJ, Losos JB, Gibson-Brown JJ. 2008b. A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. Journal of Morphology 269: 129-137.
65. SAS Institute. 1997. SAS/STAT user's guide. Cary: Statistical Analysis Systems Institute.
66. Schlichting CD, Pigliucci M. 1995. Gene regulation, quantitative genetics and the evolution of reaction norms. Evolutionary Ecology 9: 154-168.
67. Shine R. 2002. Eggs in autumn: responses to declining incubation temperatures by the eggs of montane lizards. Biological Journal of the Linnean Society 76: 71-77.
68. Siegal ML, Bergman A. 2002. Waddington's canalization revisited: developmental stability and evolution. Proceedings of the National Academy of Science 99: 10528-10532.
69. Sinervo B, Doughty P, Huey RB, Zamudio K. 1992. Allometric engineering: a causal analysis of natural selection on offspring size. Science 258: 1927-1930.
70. Stearns SC. 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436-445.
71. Sultan SE, Bazzaz FA. 1993. Phenotypic plasticity in Polygonum persiceria. I. diversity and uniformity in genotypic norms of reaction to light. Evolution 47: 1009-1031.
72. Telemeco RS, Radder RS, Baird TR, Shine R. 2010. Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard. Biological Journal of the Linnean Society 100: 642-655.
73. Thompson MB, Speake BK. 2004. Egg morphology and composition. In: Deeming DC, ed. Reptilian incubation: environment, evolution and behaviour. Nottingham: Nottingham University Press, 45-74.
74. 2 gradient in Arabidopsis thaliana. American Naturalist 169: 119-140.
75. Tracy CR, Snell HL. 1985. Interrelations among water and energy relations of reptilian eggs, embryos and hatchlings. American Zoologist 25: 999-1008.
76. Troyer K. 1987. Post-hatching yolk in a lizard: internalization and contribution to growth. Journal of Herpetology 21: 102-106.
77. Turro I, Dunnington EA, Nitsan Z, Picard M, Siegel PB. 1994. Effect of yolk sac removal at hatch on growth and feeding behavior in lines of chickens differing in body weight. Growth, Development and Aging 58: 105-112.
78. Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
79. Wapstra E, Uller T, While G, Olsson M, Shine R. 2010. Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards. Journal of Evolutionary Biology 23: 651-657.
80. Warner DA, Andrews RM. 2002. Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biological Journal of the Linnean Society 76: 105-124.
81. Warner DA, Chapman MN. 2011. Does solitary incubation enhance egg water uptake and offspring quality in a lizard that produces single-egg clutches? Journal of Experimental Zoology 315: 149-155.
82. Warner DA, Jorgensen CF, Janzen FJ. 2010. Maternal and abiotic effects on egg mortality and offspring size of turtles: temporal variation in selection over 7years. Functional Ecology 24: 857-866.
83. Warner DA, Radder RS, Shine R. 2009. Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination. Physiological and Biochemical Zoology 82: 363-371.
84. Warner DA, Shine R. 2005. The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard. Evolution 59: 2209-2221.
85. Warner DA, Shine R. 2007. Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154: 65-73.
86. Warner DA, Shine R. 2008. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451: 566-568.
87. Warner DA, Shine R. 2009. Maternal and environmental effects on offspring phenotypes in an oviparous lizard: do field data corroborate laboratory data? Oecologia 161: 209-220.
88. Warner DA, Shine R. 2011. Interactions among thermal parameters determine offspring sex under temperature-dependent sex determination. Proceedings of the Royal Society B 278: 256-265.
89. Weiss SL, Johnston G, Moore MC. 2007. Corticosterone stimulates hatching of late-term tree lizard embryos. Comparative Biochemistry and Physiology A 146: 360-365.
90. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford: Oxford University Press.
91. Willette DAS, Tucker JK, Janzen FJ. 2005. Linking climate and physiology at the population level for a key life-history stage of turtles. Canadian Journal of Zoology 83: 845-850.