High food abundance permits the evolution of placentotrophy: Evidence from a placental lizard, Pseudemoia entrecasteauxii

American Naturalist

Volumn 184, Issue 2, 2014, Pages 198-210

  Van Dyke, James U ^a   Griffith, Oliver W ^a   Thompson, Michael B ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cannibalism; Life history evolution; Matrotrophy; Parent offspring conflict; Reproduction; Viviparity

Indexed keywords

ANIMAL; ANIMAL EMBRYO; ANIMAL FOOD; CANNIBALISM; EMBRYOLOGY; EVOLUTION; FEMALE; GROWTH, DEVELOPMENT AND AGING; LIZARD; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; VIVIPARITY;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BIOLOGICAL EVOLUTION; CANNIBALISM; EMBRYO, NONMAMMALIAN; FEMALE; LIZARDS; PLACENTA; PREGNANCY; VIVIPARITY, NONMAMMALIAN;

EID: 84904816403     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/677138     Document Type: Article

References (71)

1. Adams, S. M., J. M. Biazik, M. B. Thompson, and C. R. Murphy. 2005. Cyto-epitheliochorial placenta of the viviparous lizardPseudemoia entrecasteauxii: a new placental morphotype. Journal of Morphology 264:264-276.
2. Banet, A. I., A. G. Au, and D. Reznick. 2010. Is mom in charge? implications of resource provisioning on the evolution of the placenta. Evolution 64:3172-3182.
3. Banet, A. I., and D. N. Reznick. 2008. Do placental species abort offspring? testing an assumption of the Trexler-DeAngelis model. Functional Ecology 22:323-331.
4. Bassar, R. D., S. K. Auer, and D. Reznick. 2014. Why do placentas evolve? a test of the life-history facilitation hypothesis in two clades in the genus Poeciliopsisrepresenting two independent origins of placentas. Functional Ecology. doi:10.1111/1365-2435.12233.
5. Bauwens, D., and C. Thoen. 1981. Escapetactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. Journal of Animal Ecology 50:733-743.
6. Biazik, J. M., M. B. Thompson, and C. R. Murphy. 2009. Lysosomal and alkaline phosphatase activity indicate macromolecule transport across the uterine epithelium in two viviparous skinks with complex placenta. Journal of ExperimentalZoology B: Molecular and Developmental Evolution 312:817-826.
7. Blackburn, D. G. 1992. Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. American Zoologist 32:313-321.
8. Blackburn, D. G. 1994. Standardized criteria for therecognition of embryonic nutritional patterns in squamate reptiles. Copeia 1994:925-935.
9. Blackburn, D. G. 2014. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. Journal of Morphology. doi:10.1002/jmor.20272.
10. Blackburn, D. G., and A. F. Flemming. 2012. Invasive implantation and intimate placental associations in a placentotrophic African lizard, Trachylepis ivensi(Scincidae). Journal of Morphology 273: 137-159.
11. Blackburn, D. G., K. K. Weaber, J. R. Stewart, and M. B. Thompson. 2003. Do pregnant lizards resorb or abort inviable eggs and embryos? morphological evidence from an Australian skink, Pseudemoia pagenstecheri. Journal of Morphology 256:219-234.
12. Bonnet, X., O. Lourdais, R. Shine, and G. Naulleau. 2002. Reproduction in a typical capital breeder: costs, currencies, and complications in the aspic viper. Ecology 83:2124-2135.
13. Brown, G. W. 1988. The diet ofLeiolopisma entrecasteauxii(Lacertilia, Scincidae) from southwestern Victoria, with notes on its relationship with the reproductive-cycle. Australian Wildlife Research 15: 605-614.
14. Clark, D. R. 1971. The strategy of tail-autotomy in the ground skink, Lygosoma laterale. Journal of Experimental Zoology 176:295-302.
15. Crespi, B., and C. Semeniuk. 2004. Parent-offspring conflict in the evolution of vertebrate reproductive mode. American Naturalist 163:635-653.
16. Dulvy, N. K., and J. D. Reynolds. 1997. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proceedings of the Royal Society B: Biological Sciences 264: 1309-1315.
17. Dunham, A. E., B. W. Grant, and K. L. Overall. 1989. Interfaces between biophysical and physiological ecology, andthe population ecology of terrestrial vertebrate ectotherms. Physiological Zoology 62:335-355.
18. Flemming, A. F., and D. G. Blackburn. 2003. Evolution of placental specializations in viviparous African and South American lizards. Journal of Experimental Zoology A: Comparative Experimental Biology 299:33-47.
19. Gignac, A., and P. T. Gregory. 2005. The effects of body size, age, and food intake during pregnancy on reproductive traits of a viviparous snake, Thamnophis ordinoides. Ecoscience 12:236-243.
20. Gregory, P. T., L. H. Crampton, and K. M. Skebo. 1999. Conflicts and interactions among reproduction, thermoregulation and feeding in viviparous reptiles: are gravid snakes anorexic? Journal of Zoology 248:231-241.
21. Gregory, P. T., and K. M. Skebo. 1998. Trade-offs between reproductive traits and the influence of food intake during pregnancy in the garter snake, Thamnophis elegans. American Naturalist 151: 477-486.
22. Griffith, O. W., B. Ujvari, K. Belov, and M. B. Thompson. 2013a. Placental lipoprotein lipase (LPL) gene expression in a placentotrophic lizard, Pseudemoia entrecasteauxii. Journal of Experimental Zoology B: Molecular and Developmental Evolution 320:465-470.
23. Griffith, O. W., J. U. Van Dyke, and M. B. Thompson. 2013b. No implantation in an extrauterine pregnancy of a placentotrophic reptile. Placenta 34:510-511.
24. Hare, K. M., and A. Cree. 2010. Incidence, causes and consequences of pregnancy failure in viviparous lizards: implications for research and conservation settings. Reproduction, Fertility, and Development 22:761-770.
25. Itonaga, K., S. M. Jones, and E. Wapstra. 2012a. Do gravid females become selfish? female allocation of energy during gestation. Physiological and Biochemical Zoology 85:231-242.
26. Itonaga, K., S. M. Jones, and E. Wapstra. 2012b. Effects of maternal basking and food quantity during gestation provide evidence for the selective advantage of matrotrophy in a viviparous lizard. PLoS ONE 7:e41835.
27. Jung, S., D. A. Rickert, N. A. Deak, E. D. Aldin, J. Recknor, L. A. Johnson, and P. A. Murphy. 2003. Comparison of Kjeldahl and Dumas methods for determining protein contents of soybean products. Journal of the American Oil Chemists' Society 80:1169-1173.
28. Lourdais, O., X. Bonnet, and P. Doughty. 2002. Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis). Journal of Experimental Zoology 292:487-493.
29. Lourdais, O., F. Brischoux, D. DeNardo, and R. Shine. 2004. Protein catabolism in pregnant snakes (Epicrates cenchria maurusBoidae) compromises musculature and performance after reproduction. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 174:383-391.
30. Lourdais, O., F. Brischoux, R. Shine, and X. Bonnet. 2005. Adaptive maternal cannibalism in snakes (Epicrates cenchria maurus, Boidae). Biological Journal of the Linnean Society 84:767-774.
31. Marsh-Matthews, E., and R. Deaton. 2006. Resources and offspring provisioning: a test of the Trexler-DeAngelis model for matrotrophy evolution. Ecology 87:3014-3020.
32. Moore, T. 2012. Parent-offspring conflict and the control of placental function. Placenta 33(suppl.):S33-S36.
33. Murphy, K., S. Hudson, and G. Shea. 2006. Reproductive seasonality of three cold-temperate viviparous skinks from southeastern Australia. Journal of Herpetology 40:454-464.
34. Pires, M. N., J. Arendt, and D.N. Reznick. 2010. The evolution of placentas and superfetation in the fish genusPoecilia(Cyprinodontiformes: Poeciliidae: subgeneraMicropoeciliaand Acanthophacelus). Biological Journal of the Linnean Society 99:784-796.
35. Pollux, B. J. A., and D. N. Reznick. 2011. Matrotrophy limits a female's ability to adaptively adjust offspring size and fecundity in fluctuating environments. Functional Ecology25:747-756.
36. Ramirez-Pinilla, M. P. 2006. Placental transfer of nutrients during gestation in an Andean population of the highly matrotrophic lizard genusMabuya(Squamata: Scincidae). Herpetological Monographs 20:194-204.
37. Ramirez-Pinilla, M. P., V. H. Serrano, and J. C. Galeano. 2002. Annual reproductive activity ofMabuya mabouya(Squamata, Scincidae). Journal of Herpetology 36:667-677.
38. Reznick, D., M. Mateos, and M. S. Springer. 2002. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298:1018-1020.
39. Riesch, R., R. A. Martin, and R. B. Langerhans. 2013. Predation's role in life-history evolution of a livebearing fish and a test of the Trexler-DeAngelis model of maternal provisioning. American Naturalist 181:78-93.
40. Robert, K. A., and M. B. Thompson.2000. Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development. Comparative Biochemistry andPhysiology A: Molecular and Integrative Physiology 127:481-486.
41. Scheiner, S. M. 2001. MANOVA: multiple response variables and multispecies interactions. Pages 99-115in S. M. Scheiner and J. Gurevitch, eds. Design and Analysis of Ecological Experiments. Oxford University Press, New York.
42. Shine, R. 1980. "Costs" of reproduction in reptiles. Oecologia (Berlin) 46:92-100.
43. Shine, R., and S. J. Downes. 1999. Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia (Berlin) 119:1-8.
44. Sinervo, B. 1990. The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance. Evolution 44:279-294.
45. Stapley, J., C. M. Hayes, and S. J. Keogh. 2003. Population genetic differentiation and multiple paternitydetermined by novel microsatellite markers from the mountain log skink (Pseudemoia entrecasteauxii). Molecular Ecology Notes 3:291-293.
46. Stewart, J. R. 1989. Facultative placentotrophyand the evolution of squamate placentation: quality of eggs and neonates in Virginia striatula. American Naturalist 133:111-137.
47. Stewart, J. R., and M. B. Thompson. 1993. A novel pattern of embryonic nutrition in a viviparous reptile. Journal of Experimental Biology 174:97-108.
48. Stewart, J. R., and M. B. Thompson. 1996. Evolution of reptilian placentation: development of extraembryonic membranes of the Australian scincid lizards, Bassiana duperreyi (Oviparous) and Pseudemoia entrecasteauxii(Viviparous). Journal of Morphology 227:349-370.
49. Stewart, J. R., and M. B. Thompson. 2009. Parallel evolution of placentation in Australian Scincid lizards. Journal of Experimental Zoology B: Molecular and Developmental Evolution 312:590-602.
50. Swain, R., and S. M. Jones. 2000. Facultative placentotrophy: halfway house or strategic solution? Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 127:441-451.
51. Thompson, M. B., and B. K. Speake. 2003. Energy and nutrient utilisation by embryonic reptiles. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 133:529-538.
52. Thompson, M. B., and B. K. Speake. 2006. A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 176:179-189.
53. Thompson, M. B., B. K. Speake, J. R. Stewart, K. J. Russell, and R. J. McCartney. 2001. Placental nutrition in the Tasmanian skink, Niveoscincus ocellatus. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 171:155-160.
54. Thompson, M. B., B. K. Speake, J. R. Stewart, K. J. Russell, R. J. McCartney, and P. F. Surai. 1999a. Placental nutrition in the viviparous lizardNiveoscincus metallicus: the influence of placental type. Journal of Experimental Biology 202:2985-2992.
55. Thompson, M. B., J. R. Stewart, and B. K. Speake. 2000. Comparison of nutrient transport across the placenta of lizards differing in placental complexity. Comparative Biochemistryand Physiology A: Molecular and IntegrativePhysiology 127:469-479.
56. Thompson, M. B., J. R. Stewart, B. K. Speake, K. J. Russell, and R. J. McCartney. 1999b. Placental transfer of nutrients during gestation in the viviparous lizard, Pseudemoia spenceri. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 169:319-328.
57. Thompson, M. B., J. R. Stewart, B. K. Speake, K. J. Russell, R. J. McCartney, and P. F. Surai. 1999c. Placental nutrition in a viviparous lizard (Pseudemoia pagenstecheri) with a complex placenta. Journal of Zoology 248:295-305.
58. Tinkle, D. W., and J. W. Gibbons. 1977. The distribution and evolution of viviparity in reptiles. Miscellaneous publication no. 154. Museum of Zoology, University of Michigan, Ann Arbor.
59. Trexler, J. C. 1985. Variation in the degree of viviparity in the sailfin molly, Poecilia latipinna. Copeia 1985:999-1004.
60. Trexler, J. C., and D. L. DeAngelis.2003. Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy. American Naturalist 162:574-585.
61. Van Dyke, J. U., and S. J. Beaupre. 2011. Bioenergetic components of reproductive effort in viviparoussnakes: costs of vitellogenesis exceed costs of pregnancy. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 160:504-515.
62. Van Dyke, J. U., and S. J. Beaupre. 2012. Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation. Journal of Experimental Biology 215:760-765.
63. Van Dyke, J. U., S. J. Beaupre, and D.L. Kreider. 2012. Snakes allocate amino acids acquired during vitellogenesis to offspring: are capital and income breeding consequences of variable foraging success? Biological Journal of the Linnean Society 106:390-404.
64. Van Dyke, J. U., M. C. Brandley, and M. B. Thompson. 2014a. The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes. Reproduction 147:R15-R26.
65. Van Dyke, J. U., O. W. Griffith, and M. B. Thompson. 2014b. Data from: High food abundance permits the evolution of placentotrophy: evidence from a placental lizard, Pseudemoia entrecasteauxii. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.52n61.
66. Vitt, L. J., and D. G. Blackburn. 1983. Reproduction in the lizard Mabuya heathi(Scincidae): a commentary on viviparity in new worldMabuya. Canadian Journal of Zoology 61:2798-2806.
67. Vitt, L. J., and D. G. Blackburn. 1991. Ecology and life history of the viviparous lizardMabuya bistriata(Scincidae) in the Brazilian Amazon. Copeia 1991: 916-927.
68. Wake, M. H. 2014. Fetal adaptations for viviparity in amphibians. Journal of Morphology doi:10.1002/jmor.20271.
69. Wallace, R. A. 1985. Vitellogenesis and oocyte growth in nonmammalian vertebrates. Pages 127-177in L. W. Browder, ed. Developmental biology: a comprehensive synthesis. Plenum, New York.
70. Wheatley, K. E., C. J. A. Bradshaw, R. G. Harcourt, and M. A. Hindell. 2008. Feast or famine: evidence for mixed capital-income breeding strategies in Weddell seals. Oecologia (Berlin) 155:11-20.
71. Wourms, J. P. 1981. Viviparity: the maternal-fetal relationship in fishes. American Zoologist 21:473-515.