Eggshell morphology and gekkotan life-history evolution

Evolutionary Ecology - Tập 26 - Trang 847-861 - 2011
David A. Pike1, Robin M. Andrews2, Wei-Guo Du3
1School of Marine and Tropical Biology, James Cook University, Townsville, Australia
2Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, USA
3Key Laboratory of Animal Ecology and Conservational Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

Tóm tắt

Eggshell structure is related to fundamental aspects of embryonic development (via water and gas exchange), adult ecology and behavior (via nest site selection), and demography (via effects on survival). We compared life-history characteristics between gekkotans that lay rigid- versus parchment- shelled eggs to determine if evolutionary shifts in eggshell structure are associated with life-history evolution. Ancestral gekkotans laid parchment-shelled eggs, with rigid-shelled eggs evolving later. Clutch size in oviparous gekkotans is fixed at one or two eggs, and this characteristic eliminates an egg size versus clutch size tradeoff as a life-history strategy. We found that species laying rigid-shelled eggs exhibit (1) smaller eggs relative to adult body size, (2) smaller hatchlings relative to the size of the egg, (3) earlier embryonic stage at oviposition, (4) longer incubation periods, and (5) smaller adult body sizes than species laying parchment-shelled eggs. These patterns hold when accounting for phylogenetic relatedness, and are not explained by geographic distributions of climate and habitat. In general, our data support the hypothesis that the spherical shapes of rigid-shelled eggs limit their size (volume), which in turn has restricted hatchling size and adult body size. In contrast, while parchment-shelled eggs are similarly constrained in width, elongate shapes allow egg sizes, and hence hatchling sizes, to increase relative to adult body sizes. Finally, the evolution of rigid-shelled eggs may have allowed gekkotans to become so successful; over 1,000 species lay rigid-shelled eggs, as compared to about 200 species that lay eggs exhibiting the ancestral parchment-shelled condition.

Tài liệu tham khảo

Ackerman RA, Seagrave RC, Dmi’el R, Ar A (1985) Water and heat exchange between parchment-shelled reptile eggs and their surroundings. Copeia 1985:703–711 Andrews RM (1982) Patterns of growth in reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia. Vol 13 Physiology D: physiological ecology. Academic Press, New York, pp 273–320 Andrews R (2004) Patterns of embryonic development. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 75–102 Annable TJ (2004) Reproductive biology of Nephrurus and Underwoodisaurus gekkotans (Reptilia: Gekkonidae: Carphodactylini). Unpublished PhD thesis, The University of Sydney Bain MM (1991) A reinterpretation of eggshell strength. In: Solomon SE (ed) Egg and eggshell quality. Wolfe Publishing Limited, Aylesbury, pp 131–145 Bauwens D, Díaz-Uriarte R (1997) Covariation of life-history traits in lacertid lizards: a comparative study. Am Nat 149:91–111 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 University Press, Nottingham, pp 125–141 Bomford M, Kraus F, Barry SC, Lawrence E (2009) Predicting establishment success for alien reptiles and amphibians: a role for climate matching. Biol Inv 11:713–724 Bond JE, Opell BD (1998) Testing adaptive radiation and key innovation hypotheses in spiders. Evolution 52:403–414 Branch B (1998) Field guide to snakes and other reptiles of Southern Africa. Ralph Curtis Publishing, Florida Brown WC, Alcala AC (1957) Viability of lizard eggs exposed to sea water. Copeia 1957:39–41 Brown SG, Duffy PK (1992) The effects of egg-laying site, temperature, and salt water on incubation time and hatching success in the gekkotan Lepidodactylus lugubris. J Herpetol 26:510–513 Carranza S, Arnold EN, Mateo JA, Lopez-Jurado LF (2000) Long-distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: Gekkonidae), revealed by mitochondrial DNA sequences. Proc R Soc Lond B 267:637–649 Congdon JD, Gibbons JW (1987) Morphological constraint on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci 84:4145–4147 Cronin ER, Seymour RS (2000) Respiration of the eggs of the giant cuttlefish Sepia apama. Marine Biol 136:863–870 Deeming DC (1988) Eggshell structure of lizards of two sub-families of the Gekkonidae. Herpetol J 1:230–234 Deeming DC, Thompson MB (1991) Gas exchange across reptilian eggshells. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 277–284 Deeming DC, Unwin DM (2004) Reptilian incubation: evolution and the fossil record. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 1–14 Doughty P (1997) The effects of “fixed” clutch sizes on lizard life-histories: reproduction in the Australian velvet gekkotan, Oedura lesueurii. J Herpetol 31:266–272 Dufaure JP, Hubert J (1961) Table de de’veloppment du le’zard vivipare: Lacerta (Zootica) vivipara Jaquin. Arch Anat Microsc Mo 50:309–328 Dunson WA (1982) Low water vapor conductance of hard-shelled eggs of the gekkotan lizards Hemidactylus and Lepidodactylus. J Exp Zool 219:377–379 Felsenstein J (1997) Phylogenies and the comparative method. Am Nat 125:1–15 Gamble T, Bauer AM, Greenbaum E, Jackman TR (2008) Out of the blue: a novel trans-Atlantic clade of gekkotans (Gekkota, Squamata). Zool Scrip 37:355–366 Gardner AS (1985) Viability of the eggs of the day-gekkotan Phelsuma sundbergi exposed to sea water. Br J Herpetol 6:435–436 Greer AE (1989) The biology and evolution of Australian lizards. Surrey Beatty, New South Wales Henkel WF, Schmidt W (1995) Geckoes: biology, husbandry and reproduction. Krieger Publishing, Florida Henle K (1990) Population ecology and life history of arboreal gecko Gehyra variegata in arid Australia. Herpetol Monogr 4:30–60 Ineich I (2010) How habitat disturbance benefits gekkotans: conservation implications. Comptes Rendus Biol 444:76–82 Iverson JB, Ewert MA (1991) Physical characteristics of reptilan eggs and a comparison with avian eggs. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 87–100 Köhler G (2005) Incubation of reptile eggs. Krieger Publishing, Florida Kratochvíl L, Frynta D (2006) Egg shape and size allometry in gekkotans (Squamata: Gekkota), lizards with contrasting eggshell structure: why lay spherical eggs? J Zool Syst Evol Res 44:217–222 Kratochvíl L, Kubicka L (2007) Why reduce clutch size to one or two eggs? Reproductive allometries reveal different evolutionary causes of invariant clutch size in lizards. Funct Ecol 21:171–177 Maddison WP, Maddison DR (2006) Mesquite: a modular system for evolutionary analysis. Version 1.1. http://www.mesquiteproject.org Michoud EJ, Echternacht AC (1995) Geographic variation in the life history of the lizard Anolis carolinensis and support for the pelvic constraint model. J Herpetol 29:86–97 Midford PE, Garland T Jr, Maddison WP (2005) PDAP package of mesquite. Version 1.07 Moreira PL, Barata M (2005) Egg mortality and early embryo hatching caused by fungal infection of Iberian rock lizard (Lacerta monticula) clutches. Herpetol J 15:265–272 Oftedal OT (2002) The origin of lactation as a water source for parchment-shelled eggs. J Mammary Gland Biol Neoplasia 17:253–266 Osadnik G (1984) An investigation of egg laying in Phelsuma (Reptilia: Sauria: Gekkonidae). Ampibia-Reptilia 5:125–134 Packard GC (1991) The physiological and ecological importance of water to embryos of oviparous reptiles. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 213–228 Packard MJ, DeMarco VG (1991) Eggshell structure and formation in eggs of oviparous reptiles. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 53–69 Packard GC, Packard MJ (1988) The physiological ecology of reptilian eggs and embryos. In: Gans C, Huey RB (eds) Biology of the reptilia, vol 16, defense and life history, Alan R. Liss Inc., New York, pp 523–605 Packard MJ, Seymour RS (1997) Evolution of the amniote egg. In: Sumida SS, Martin KLM (eds) Amniote origins: completing the transition to land. Academic Press, New York, pp 265–290 Pike DA, Webb JK, Shine R (2010) Nesting in a thermally challenging environment: nest site selection in a rock-dwelling gecko, Oedurea lesueurii (Reptilia: Gekkonidae). Biol J Linn Soc 99:250–259 Pough FH, Andrews RM, Cadle JE, Crump ML, Savitzky AH, Wells KD (2004) Herpetology. Prentice-Hall, New Jersey Schleich HH, Kästle W (1988) Reptile egg-shells SEM stlas. Gustav Fischer, Stuttgart Shattuck M, Williams SA (2010) Arboreality has allowed for the evolution of increased longevity in mammals. P Natl Acad Sci USA 107:4635–4639 Shedlock AM, Edwards SV (2009) Amniotes (Amniota). In: Hedges SB, Kumar S (eds) Timetree of life. Oxford University Press, Oxford, pp 375–379 Simbotwe MP (1983) Comparative ecology of diurnal gekkotans (Lygodactylus) in Kafue flats, Zambia. Afr J Ecol 21:143–153 Sinervo B, Licht P (1991) Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252:1300–1302 Stewart JR (1997) Morphology and evolution of the egg of oviparous amniotes. In: Sumida SS, Martin KLM (eds) Amniote origins: completing the transition to land. Academic Press, New York, pp 291–326 Thompson MB, Russell KJ (1999) Growth and energetics of embryos of the gekkotan, Phyllodactylus marmoratus, a species with hard-shelled eggs. Herpetol J 9:37–42 Thompson MB, Speake BK (2004) Egg morphology and composition. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 45–74 Warne RW, Charnov EL (2008) Reproductive allometry and the size-number trade-off for lizards. Am Nat 172:E80–E98 Wise PAD, Vickaryous MK, Russell AP (2009) An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko. Anat Rec 292:1198–1212 Xu D–D, Ji X (2007) Sexual dimorphism, female reproduction and egg incubation in the oriental leaf-toed gekkotan (Hemidactylus bowringii) from southern China. Zoology 110:20–27 Zhang Y-P, Du W-G, Zhu L-J (2009) Differences in body size and female reproductive traits between two sympatric gekkotans: Gekko japonicus and Gekko hokouensis. Folia Zool 58:113–122 Zhao EM, Zhao KT, Zhou KY (1999) Fauna Sinica Reptilia, vol 2: Squamata. Chinese Science Press, Beijing