Skip to main content
Log in

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

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

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, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

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

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  PubMed  Google Scholar 

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

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

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

  • Jirtle RL (2006) Geneimprint

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

  • 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 

  • 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

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

  • 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 

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

    Article  CAS  Google Scholar 

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

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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

    Article  CAS  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

Authors and 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

Check for updates. 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

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-016-0531-x

Keywords

Navigation