Allelic expression of mammalian imprinted genes in a matrotrophic lizard, Pseudemoia entrecasteauxii

Abstract

Genomic imprinting is a process that results in the differential expression of genes depending on their parent of origin. It occurs in both plants and live-bearing mammals, with imprinted genes typically regulating the ability of an embryo to manipulate the maternal provision of nutrients. Genomic imprinting increases the potential for selection to act separately on paternally and maternally expressed genes, which increases the number of opportunities that selection can facilitate embryonic control over maternal nutrient provision. By looking for imprinting in an independent matrotrophic lineage, the viviparous lizard Pseudemoia entrecasteauxii (Scincidae), we test the hypothesis that genomic imprinting facilitates the evolution of substantial placental nutrient transport to embryos (matrotrophy). We sequenced transcriptomes from the embryonic component of lizard placentae to determine whether there are parent-of-origin differences in expression of genes that are imprinted in mammals. Of these genes, 19 had sufficiently high expression in the lizard to identify polymorphisms in transcribed sequences. We identified bi-allelic expression in 17 genes (including insulin-like growth factor 2), indicating that neither allele was imprinted. These data suggest that either genomic imprinting has not evolved in this matrotrophic skink or, if it has, it has evolved in different genes to mammals. We outline how these hypotheses can be tested. This study highlights important differences between mammalian and reptile pregnancy and the absence of any shared imprinting genes reflects fundamental differences in the way that pregnancy has evolved in these two lineages.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Angiolini E, Fowden A, Coan P, Sandovici I, Smith P, Dean W, Burton G, Tycko B, Reik W, Sibley C et al. 2006. Regulation of placental efficiency for nutrient transport by imprinted genes. Placenta 27, Supplement: 98–102.

  3. Blackburn DG (2014) Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J Morphol 276:961–990

    Article  PubMed  Google Scholar 

  4. Blackburn D (2015) Viviparous placentotrophy in reptiles and the parent–offspring conflict. J Exp Zool Part B 324:532–548

    Article  Google Scholar 

  5. Brandley MC, Young RL, Warren DL, Thompson MB, Wagner GP (2012) Uterine gene expression in the live-bearing lizard, Chalcides ocellatus, reveals convergence of squamate reptile and mammalian pregnancy mechanisms. Genome Biol Evol 4:394–411

    Article  PubMed  PubMed Central  Google Scholar 

  6. Crespi B, Semeniuk C (2004) Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am Nat 163:635–653

    Article  PubMed  Google Scholar 

  7. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S et al (2015) Ensembl 2015. Nucleic Acids Res 43:D662–D669

    Article  PubMed  PubMed Central  Google Scholar 

  8. Das R, Anderson N, Koran MI, Weidman JR, Mikkelsen TS, Kamal M, Murphy SK, Linblad-Toh K, Greally JM, Jirtle RL (2012) Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica. BMC Genomics 13:1–13

    Article  Google Scholar 

  9. Dufaure JP, Hubert J (1961) Table de developpement du lezard vivipare Lacerta (Zootoca) vivipara Jacquin. Arch Anat Micr Morph Exp 50: 309–328

  10. Feil R, Berger F (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23:192–199

    CAS  Article  PubMed  Google Scholar 

  11. Feil R, Khosla S (1999) Genomic imprinting in mammals: an interplay between chromatin and DNA methylation? Trends Genet 15:431–435

    CAS  Article  PubMed  Google Scholar 

  12. Frésard L, Leroux S, Servin B, Gourichon D, Dehais P, Cristobal MS, Marsaud N, Vignoles F, Bed’hom B, Coville J-L et al (2014) Transcriptome-wide investigation of genomic imprinting in chicken. Nucleic Acids Res 42:3768–3782

    Article  PubMed  PubMed Central  Google Scholar 

  13. Graves JAM, Renfree MB (2013) Marsupials in the age of genomics. Annu Rev Genomics Hum Genet 14:393–420

    Article  PubMed  Google Scholar 

  14. Griffith OW (2015) Mechanisms of placental evolution: the genetics and physiology of pregnancy in lizards. University of Sydney, Sydney, Australia

  15. Griffith OW, Ujvari B, Belov K, Thompson MB (2013a) Placental lipoprotein lipase (LPL) gene expression in a placentotrophic lizard. Pseudemoia entrecasteauxii J Exp Zool Part B 320:465–470

    CAS  Google Scholar 

  16. Griffith OW, Van Dyke JU, Thompson MB (2013b) No implantation in an extra-uterine pregnancy of a placentotrophic reptile. Placenta 34:510–511

    CAS  Article  PubMed  Google Scholar 

  17. Griffith OW, Blackburn DG, Brandley MC, Van Dyke JU, Whittington CM, Thompson MB (2015) Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: a case study examining the evolution of reproductive mode in squamate reptiles. J Exp Zool Part B 324:493–503

    Article  Google Scholar 

  18. Haig D (1999) Multiple paternity and genomic imprinting. Genetics 151:1229–1231

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Haig D (2000) The kinship theory of genomic imprinting. Annu Rev Ecol Syst 31: 9–32

  20. Haig D, Graham C (1991) Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell 64:1045–1046

    CAS  Article  PubMed  Google Scholar 

  21. Haig D, Westoby M (1991) Genomic imprinting in endosperm - its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philos T Roy Soc B 333B:1–13

    Article  Google Scholar 

  22. Hoffman LH (1970) Placentation in the garter snake, Thamnophis sirtalis. J Morphol 131:57–87

    CAS  Article  PubMed  Google Scholar 

  23. Holman L, Kokko H (2014) The evolution of genomic imprinting: costs, benefits and long-term consequences. Biol Rev 89:568–587

    Article  PubMed  Google Scholar 

  24. Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680–682

  25. Itonaga K, Jones SM, Wapstra E (2012) Do gravid females become selfish? Female allocation of energy during gestation. Physiol Biochem Zool 85: 231–242

  26. Jirtle RL (2006) Geneimprint

  27. Killian JK, Nolan CM, Stewart N, Munday BL, Andersen NA, Nicol S, Jirtle RL (2001) Monotreme IGF2 expression and ancestral origin of genomic imprinting. J Exp Zool 291:205–212

    CAS  Article  PubMed  Google Scholar 

  28. Lawton BR, Sevigny L, Obergfell C, Reznick D, O’Neill RJ, O’Neill MJ (2005) Allelic expression of IGF2, in live-bearing, matrotrophic fishes. Dev Genes Evol 215:207–212

    CAS  Article  PubMed  Google Scholar 

  29. Lawton BR, Carone BR, Obergfell CJ, Ferreri GC, Gondolphi CM, Vandeberg JL, Imumorin I, O’Neill RJ, O’Neill MJ (2008) Genomic imprinting of IGF2 in marsupials is methylation dependent. BMC Genomics 9

  30. Moore T, Haig D (1991) Genomic imprinting in mammalian development—a parental tug-of-war. Trends Genet 7:45–49

    CAS  Article  PubMed  Google Scholar 

  31. Murphy BF, Parker SL, Murphy CR, Thompson MB (2010) Angiogenesis of the uterus and chorioallantois in the eastern water skink Eulamprus quoyii. J Exp Biol 213:3340–3347

    Article  PubMed  Google Scholar 

  32. O’Neill MJ, Ingram RS, Vrana PB, Tilghman SM (2000) Allelic expression of IGF2 in marsupials and birds 210:18–20.

  33. O’Neill MJ, Lawton BR, Mateos M, Carone DM, Ferreri GC, Hrbek T, Meredith RW, Reznick DN, O’Neill RJ (2007) Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes. Proc Natl Acad Sci U S A 104:12404–12409

    Article  PubMed  PubMed Central  Google Scholar 

  34. Pask A, Papenfuss A, Ager E, McColl K, Speed T, Renfree M. 2009. Analysis of the platypus genome suggests a transposon origin for mammalian imprinting. Genome Biol 10: 10.1186/gb-2009-1110-1181-r1181

  35. Prickett AR, Oakey RJ (2012) A survey of tissue-specific genomic imprinting in mammals 287:621–630

  36. Rademacher K, Schröder C, Kanber D, Klein-Hitpass L, Wallner S, Zeschnigk M, Horsthemke B (2014) Evolutionary origin and methylation status of human intronic CpG islands that are not present in mouse. Genome Biol Evol 6:1579–1588

    Article  PubMed  PubMed Central  Google Scholar 

  37. Reik W, Walter J (1998) Imprinting mechanisms in mammals. Curr Opin Genetics Dev 8:154–164

    CAS  Article  Google Scholar 

  38. Renfree MB, Ager EI, Shaw G, Pask AJ. 2008. Genomic imprinting in marsupial placentation. 136: 523–531

  39. Renfree MB, Suzuki S, Kaneko-Ishino T (2013) The origin and evolution of genomic imprinting and viviparity in mammals. P Roy Soc B-Biol Sci 368

  40. Sasaki H, Ishihara K, Kato R (2000) Mechanisms of Igf2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. J Biochem 127:711–715

    CAS  Article  PubMed  Google Scholar 

  41. Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    CAS  PubMed  Google Scholar 

  42. Speake BK, Herbert JF, Thompson MB (2004) Evidence for placental transfer of lipids during gestation in the viviparous lizard, Pseudemoia entrecasteauxii. Comp Biochem Phys A 139A:213–220

    CAS  Article  Google Scholar 

  43. Spencer HG, Clark AG (2014) Non-conflict theories for the evolution of genomic imprinting. Heredity 113:112–118

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Stapley J, Hayes CM, Scott KJ (2003) Population genetic differentiation and multiple paternity determined by novel microsatellite markers from the mountain log skink (Pseudemoia entrecasteauxii). Mol Ecol Notes 3:291–293

    CAS  Article  Google Scholar 

  45. Stewart JR, Thompson MB (1993) A novel pattern of embryonic nutrition in a viviparous reptile. J Evolution Biol 174:97–108

    Google Scholar 

  46. Stringer JM, Pask AJ, Shaw G, Renfree MB (2014) Post-natal imprinting: evidence from marsupials. Heredity 113:145–155

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Surani MA, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548

    CAS  Article  PubMed  Google Scholar 

  48. Thompson MB, Speake BK (2006) A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. J Comp Physiol 176B:179–189

    Article  Google Scholar 

  49. Thorvaldsen JL, Duran KL, Bartolomei MS (1998) Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev 12:3693–3702

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Van Dyke JU, Beaupre SJ (2012) Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation. J Exp Biol 215:760–765

    Article  PubMed  Google Scholar 

  51. Van Dyke JU, Brandley MC, Thompson MB (2014a) The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes. Reproduction 147:R15–R26

    Article  PubMed  Google Scholar 

  52. Van Dyke JU, Griffith OW, Thompson MB (2014b) High food abundance permits the evolution of placentotrophy: evidence from a placental lizard, Pseudemoia entrecasteauxii. Am Nat 184:198–210

    Article  PubMed  Google Scholar 

  53. Wang X, Miller DC, Harman R, Antczak DF, Clark AG (2013) Paternally expressed genes predominate in the placenta. Proc Natl Acad Sci USA 110: 10705–10710

  54. Whittington CM, Griffith OW, Qi W, Thompson MB, Wilson AB (2015) Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. Mol Biol Evol 32:3114–3131

    PubMed  Google Scholar 

  55. Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4:359–368

    CAS  Article  PubMed  Google Scholar 

  56. Wolf JB, Hager R (2006) A maternal–offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol 4:e380

    Article  PubMed  PubMed Central  Google Scholar 

  57. Wright A, Lyons K, Brandley MC, Hillis DM (2015) Which came first: the lizard or the egg? Robustness in phylogenetic reconstruction of ancestral states. J Exp Zool B Mol Dev Evol 324:504–516

    Article  PubMed  Google Scholar 

  58. Yu JYL, Dickhoff WW, Swanson P, Gorbman A (1981) Vitellogenesis and its hormonal regulation in the Pacific hagfish, Eptatretus stouti L. Gen Comp Endocrinol 43:492–502

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

Lizards were collected under New South Wales National Parks and Wildlife Licence to MBT (SL100401). We thank Intersect Australia Ltd. for supercomputing resources as well as Bosch MBF and M. Olsson for laboratory resources. This project was supported by The Australian Society of Herpetologist’s student research grant and the Gaylord Donnelley Postdoctoral Environmental Fellowship to OWG, Australian Research Council Discovery Early Career Research Award to MCB (DE120101615), and ARC Discovery Project funding to MBT (DP120100649).

Author contributions

OWG performed pyrosequencing, data analyses, and wrote the manuscript. OWG and MCB collected lizards and constructed RNA-seq libraries. MBT, MCB, KB, and OWG contributed to development of the ideas and conclusions, experimental design, and editing of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Oliver W. Griffith.

Ethics declarations

Animal work was conducted under University of 441 Sydney Animal Ethic approval.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Andreas Kispert

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 65 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Griffith, O.W., Brandley, M.C., Belov, K. et al. Allelic expression of mammalian imprinted genes in a matrotrophic lizard, Pseudemoia entrecasteauxii . Dev Genes Evol 226, 79–85 (2016). https://doi.org/10.1007/s00427-016-0531-x

Download citation

Keywords

  • Viviparity
  • Parent-offspring conflict
  • Pseudemoia
  • Placenta
  • Placentotrophy
  • Lizard
  • Scincidae
  • Genomic imprinting