Abstract
Squamate reptiles (lizards and snakes) offer a unique model system for testing hypotheses about the evolutionary transition from oviparity (egg-laying) to viviparity (live-bearing) in amniote vertebrates. The evolution of squamate viviparity has occurred remarkably frequently (>108 times) and has resulted in major changes in reproductive physiology. Such frequent changes in reproductive strategy pose two questions: (1) what are the molecular mechanisms responsible for the evolution of squamate viviparity? (2) Are these molecular mechanisms the same for separate origins of viviparity? Molecular approaches, such as RT-PCR, in situ hybridisation, Western blotting and immunofluorescence, have been invaluable for identifying genes and proteins that are involved in squamate placental development, materno-foetal immunotolerance, placental transport, placental angiogenesis, hormone synthesis and hormone receptor expression. However, the candidate-gene or -protein approach that has been used until now does not allow for de novo gene/protein discovery; results to date suggest that the reproductive physiologies of mammals and squamate reptiles are very similar, but this conclusion may simply be due to a limited capacity to study the subset of genes and proteins that are unique to reptiles. Progress has also been slowed by the lack of appropriate molecular and genomic resources for squamate reptiles. The advent of next-generation sequencing provides a relatively inexpensive way to conduct rapid high-throughput sequencing of genomes and transcriptomes. We discuss the potential use of next-generation sequencing technologies to analyse differences in gene expression between oviparous and viviparous squamates, provide important sequence information for reptiles, and generate testable hypotheses for the evolution of viviparity.
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References
Abell AJ (1998) Reproduction and post-reproductive hormone levels in the lizard Sceloporus virgatus. Acta Zool Mexicana 74:43–57
Adams SM, Biazik JM, Thompson MB, Murphy CR (2005) Cyto-epitheliochorial placenta of the viviparous lizard Pseudemoia entrecaseauxii: a new placental morphotype. J Morphol 264:264–276
Adams SM, Lui S, Jones SM, Thompson MB, Murphy CR (2007) Uterine epithelial changes during placentation in the viviparous skink Eulamprus tympanum. J Morphol 268:385–400
Adesanya OO, Zhou J, Samathanam C, Powell-Braxton L, Bondy CA (1999) Insulin-like growth factor 1 is required for g(2) progression in the estradiol-induced mitotic cycle. Proc Natl Acad Sci USA 96:3287–3291
Amey AP, Whittier JM (2000) Seasonal patterns of plasma steroid hormones in males and females of the bearded dragon lizard, Pogona barbata. Gen Comp Endocr 117:335–342
Anderson JM (2001) Molecular structure of tight junctions and their role in epithelial transport. Am Physiol Soc 16:126–130
Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotech 25:195–203
Arrayago MJ, Bea A, Heulin B (1996) Hybridization experiment between oviparous and viviparous strains of Lacerta vivipara: a new insight into the evolution of viviparity in reptiles. Herpetologica 52:333–342
Arslan M, Zaidi P, Lobo J, Zaidi AA, Qazi MH (1977) Steroid levels in preovulatory and gravid lizards (Uromastix hardwicki). Gen Comp Endocr 34:300–303
Bagot CN, Kliman HJ, Taylor HS (2001) Maternal HoxA10 is required for pinopod formation in the development of mouse uterine receptivity to embryo implantation. Dev Dynam 222:538–544
Bainbridge DRJ (2000) Evolution of mammalian pregnancy in the presence of the maternal immune system. Rev Reprod 5:67–74
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376. doi:10.1371/journal.pone.0003376
Barry M, Cockrem JF, Brunton DH (2010) Seasonal variation in plasma corticosterone concentrations in wild and captive adult Duvaucel’s geckos (Hoplodactylus duvaucelii) in New Zealand. Aust J Zool 58:234–242
Baverstock PR, Bradshaw SD (1975) Variation in rate of growth and adrenal corticosteroidogenesis in field and laboratory populations of the lizard Amphobolurus ornatus. Comp Biochem Physiol A 52:557–565
Benacerraf B (1981) Role of MHC gene products in immune regulation. Science 212:1229–1238
Bennett EJ, Jones SM (2002) Interrelationships among plasma progesterone concentrations, luteal anatomy and function, and placental ontogeny during gestation in a viviparous lizard (Niveoscincus metallicus: Scincidae). Comp Biochem Physiol A 131:647–656
Biazik JM, Thompson MB, Murphy CR (2007) The tight junctional protein occludin is found in the uterine epithelium of squamate reptiles. J Comp Physiol B 177:935–943
Biazik JM, Thompson MB, Murphy CR (2008) Claudin-5 is restricted to the tight junction region of uterine epithelial cells in the uterus of pregnant/gravid squamate reptiles. Anat Rec 291:547–556
Biazik JM, Thompson MB, Murphy CR (2009) Lysosomal and alkaline phosphatase activity indicate macromolecule transport across the uterine epithelium in two viviparous skinks with complex placenta. J Exp Zool 312B:817–826
Biazik JM, Thompson MB, Murphy CR (2010) Desmosomes in the uterine epithelium of noninvasive skink placentae. Anat Rec 293:502–512
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Greyner R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512
Blackburn DG (1993) Chorioallantoic placentation in squamate reptiles: Structure, function, development and evolution. J Exp Zool 266:414–430
Blackburn DG (1995) Saltationist and punctuated equilibrium models for the evolution of viviparity and placentation. J Theor Biol 174:199–216
Blackburn DG (1998) Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J Exp Zool 282:560–617
Blackburn DG (2006) Squamate reptiles as model organisms for the evolution of viviparity. Herpetol Monogr 20:131–146
Blackburn DG, Vitt LJ (2002) Specializations of the chorioallantoic placenta in the Brazilian scincid lizard, Mabuya heathi: a new placental morphotype for reptiles. J Morphol 254:121–131
Blackburn DG, Gavelis GS, Anderson KE, Johnson AR, Dunlap KD (2010) Placental specialisations of the mountain spiny lizard Sceloporus jarrovi. J Morphol 271:1153–1175
Bona-Gallo A, Licht P, MacKenzie DS, Lofts B (1985) Annual cycles in levels of pituitary and plasma gonadotrophin, gonadal steroids, and thyroid activity in the Chinese cobra (Naja naja). Gen Comp Endocr 42:477–493
Bonnet X, Naulleau G, Mauget R (1994) The influence of body condition on 17-β oestradiol levels in relation to vitellogenesis in female Vipera aspis (Reptilia, Viperidae). Gen Comp Endocr 93:424–437
Bonnet X, Naulleau G, Bradshaw D, Shine R (2001) Changes in plasma progesterone in relation to vitellogenesis and gestation in the viviparous snake Vipera aspis. Gen Comp Endocr 121:84–94
Botte V, Del Rio G (1965) Ricerche istochimiche sulla distribuzione dei 3α-17-chetosteroidi e di alcuni enzimi della steroidogenosi nell’ovario de Lacerta sicula. B Zool 32:191–198
Bourne AR, Stewart BJ, Watson TG (1986) Changes in blood progesterone concentration during pregnancy in the lizard Tiliqua (Trachydosaurus) rugosa. Comp Biochem Physiol A 84:581–583
Broad Institute Mammalian Genome Project website (http://www.broadinstitute.org/science/projects/mammals-models/data-release-mammalian-genome-project)
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622
Callard IP, Doolittle J, Banks WL, Chan SWC (1972) Recent studies on the control of the reptilian ovarian cycle. Gen Comp Endocr Supp 3:65–75
Callard IP, Fileti LA, Perez LE, Sorbera LA, Giannnoukos G, Klosterman LL, Paul T, McCraken JA (1992) Role of the corpus luteum and progesterone in the evolution of vertebrate viviparity. Am Zool 32:264–275
Carnevali O, Mosconi G, Angelini F, Limatola E, Ciarcia G, Polzonetti-Magni A (1991) Plasma vitellogenin and 17β-estradiol levels during the annual reproductive cycle of Podarcis s. sicula Raf. Gen Comp Endocr 84:337–343
Cartledge VA, Gartrell B, Jones SM (2005) Adrenal and white cell count responses to chronic stress in gestating and postpartum females of the viviparous skink Egernia whitii (Scincidae). Comp Biochem Physiol A 141:100–107
Cartledge VA, Jones SM (2006) Does adrenal responsiveness vary with sex and reproductive status in Egernia whitii, a viviparous skink? Gen Comp Endocr 150:132–139
Casewell NR, Harrison RA, Wuster W, Wagstaff SC (2009) Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genom 10:564
Chan SWC, Ziegel S, Callard IP (1973) Plasma progesterone in snakes. Comp Biochem Physiol A 44:631–637
Chaouat G, Zourbas S, Ostojic S, Lappree-Delage G, Dubanchet S, Ledee N, Martal J (2002) A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 53:241–256
Corso G, Delitala GM, Carcupino M (2000) Uterine morphology during the annual cycle in Chalcides ocellatus tiligugu (Gmelin) (Squamata: Scincidae). J Morphol 243:153–165
Crews D, Moore MC (2005) Historical contributions of research on reptiles to behavioural neuroendocrinology. Horm Behav 48:384–394
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalisation in Arabidopsis. Plant Physiol 139:5–17
Danielsen JMR, Sylvestersen KB, Bekker-Jensen S, Szklarczyk D, Poulsen JW, Horn H, Jensen LJ, Mailand N, Nielsen ML (2011) Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteom 10:1–12
Dauphin-Villemant C, Xavier F (1987) Nychthemeral variations of plasma corticosteroids in captive female Lacerta vivipara Jacquin: influence of stress and reproductive state. Gen Comp Endocr 67:292–302
Dauphin-Villemant C, Leboulenger F, Vaudry H (1990) Adrenal activity in the female lizard Lacerta vivipara Jacquin during artificial hibernation. Gen Comp Endocr 79:201–214
DeFalco M, Sciarrilli R, Virgilio F, Fedele V, Valiante S, Laforgia V, Varano L (2004) Annual variations of adrenal gland hormones in the lizard Podarcis sicula. J Comp Physiol A 190:675–681
Diaz JA, Alonso-Gomez AL, Delgado MJ (1994) Seasonal variation of gonadal development, sexual steroids, and lipid reserves in a population of the lizard Psammogrammus algirus. J Herpetol 28:199–205
Dunlap KD (1995) External and internal influences on indices of physiological stress: I. seasonal and population variation in adrenocortical secretion of free-living lizards, Sceloporus occidentalis. J Exp Zool 271:36–46
Ecay TW, Stewart JR, Blackburn DG (2004) Expression of calbindin-D28K by yolk sac and chorioallantoic membranes of the corn snake, Elaphe guttata. J Exp Zool 302B:517–525
Ecay TW, Fregoso S, Khambaty M, Stewart JR (2010) Developmental expression of carbonic anhydrase II in the extraembryonic membranes of oviparous and viviparous snakes. FASEB J 24:813.14
Edwards A, Jones SM (2001) Changes in plasma progesterone, estrogen, and testosterone concentrations throughout the reproductive cycle in female viviparous blue-tongued skinks, Tiliqua nigrolutea (Scincidae), in Tasmania. Gen Comp Endocr 122:260–269
Ellegren H (2008) Sequencing goes 454 and takes large-scale genomics into the wild. Mol Ecol 17:1629–1635
Enders AC, Schlafke S (1971) Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132:219–230
Endo D, Park MK (2005) Molecular cloning of P450 aromatase from the leopard gecko and its expression in the ovary. J Steroid Biochem 96:131–140
Ensembl website (http://www.ensembl.org)
Fergusson B, Bradshaw SD (1991) Plasma arginine vasotocin, progesterone, and luteal development during pregnancy in the viviparous lizard Tiliqua rugosa. Gen Comp Endocr 82:140–151
Fitch HS (1970) Reproductive cycles in lizardsa and snakes. U Kansas Mus Nat Hist Misc Pub 52:1–247
Flemming AF (1994) Seasonal variation in plasma and corpus luteum oestradiol-17β and progesterone concentrations of the lizard Cordylus p. polyzonus (Sauria: Cordylidae). S Afr J Zool 29:87–92
Fox SL, Guillette LJ (1987) Luteal morphology, atresia, and plasma progesterone concentrations during the reproductive cycle of two oviparous lizards, Crotaphytus collaris and Eumeces obsoletus. Am J Anat 179:324–332
Freire NP, Tennant MR, Miyamoto MM (2003) Microarray analyses of reptiles and amphibians: applications in ecology and evolution. Zool Stud 42:391–404
Gavaud J (1986) Vitellogenesis in the lizard Lacerta vivipara Jacquin. II. Vitellogenin synthesis during the reproductive cycle and its control by ovarian steroids. Gen Comp Endocr 63:11–23
Geraghty DE (1993) Structure of the HLA class I region and expression of its resident genes. Curr Opin Immunol 5:3–7
Girling JE (2002) The reptilian oviduct: a review of structure and function and directions for future research. J Exp Zool 293:141–170
Girling JE, Cree A (1995) Plasma corticosterone levels are not significantly related to reproductive stage in female common geckos (Hoplodactylus maculatus). Gen Comp Endocr 100:273–281
Girling JE, Jones SM, Swain R (2002) Delayed ovulation and parturition in a viviparous alipine lizard (Niveoscincus microlepidotus): morphological data and plasma steroid concentrations. Reprod Fertil Dev 14:43–53
Girling JE, Jones SM (2003) In vitro progesterone production by maternal and embryonic tissues during gestation in the southern snow skink (Niveoscincus microlepidotus). Gen Comp Endocr 133:100–108
Gorman GC, Licht P, McCollum F (1981) Annual reproductive patterns in three species of marine snakes from the central Phillipines. J Herpetol 15:335–354
Gouin N, Wright AM, Miska KB, Parra ZE, Samollov PB, Baker ML, Miller RD (2006) Modo-UG, a marsupial non-classical MHC class I locus. Immunogenetics 58:396–406
Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011
Grassman M, Crews D (1989) Ovarian and adrenal function in the parthenogenetic whiptail lizard Cnemidophorus uniparens in the field and laboratory. Gen Comp Endocr 76:444–450
Grassman M, Hess DL (1992) Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field. J Exp Zool 264:177–182
Guarino FM, Paulesu L, Cardone A, Bellini L, Ghiara G, Angelini F (1998) Endocrine activity of the corpus luteum and placenta during pregnancy in Chalcides chalcides (Reptilia, Squamata). Gen Comp Endocr 111:261–270
Guillette LJ Jr (1993) The evolution of viviparity in lizards. Bioscience 43:742–751
Guillette LJ, Spielvogel S, Moore FL (1981) Luteal development, placentation, and plasma progesterone concentration in the viviparous lizard Sceloporus jarrovi. Gen Comp Endocr 43:20–29
Guillette LJ, Jones RE (1985) Ovarian, oviductal and placental morphology of the reproductively bimodal lizard, Sceloporus aeneus. J Morphol 184:85–98
Hall N (2007) Advanced sequencing technologies and their wider impact in microbiology. J Exp Biol 209:1518–1525
Hammouche S, Gernigon TS, Exbrayat JM (2007) Immunolocalisation of estrogens and progesterone receptors within the ovary of the lizard Uromastyx acanthinura from vitellogenesis to rest season. Folia Histochem Cyto 45:23–27
Hammouche S, Gernigon T, Exbrayat JM (2009) Correlation between ovarian steroidogenesis and β-endorphin in the lizard Uromastyx acanthinura: immunohistochemical approach. Folia Histochem Cyto 47:S95–S100
Hanley KA, Petren K, Case TJ (1998) An experimental investigation of the competitive displacement of a native gecko by an invading gecko: no role for parasites. Oecologica 115:196–205
Haussler D, O’Brien SJ, Ryder OA, Barker FK, Clamp M et al (2009) Genome 10K: a proposal to obtain whole-genome sequence for 10, 000 vertebrate species. J Hered 100:659–674
Hegedus Z, Zakrzewska A, Agoston VC, Ordas A, Racz P, Mink M, Spaink HP, Meijer AH (2009) Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol Immunol 46:2918–2930
Herbert JF, Lindsay LA, Murphy CR, Thompson MB (2006) Calcium transport across the uterine epithelium of pregnant lizards. Herpetol Monogr 20:205–211
Herbert JF, Murphy CR, Thompson MB (2010) Calcium ATPase localisation in the uterus of two species of Pseudemoia (Lacertilia: Scincidae) with complex placentae. Herpetol Conserv Biol 5:290–296
Heulin B, Osenegg K, Lebouvier M (1991) Timing of embryonic development and birth dates in oviparous and viviparous strains of Lacerta vivipara: testing the predictions of an evolutionary hypothesis. Acta Oecol 12:517–528
Heulin B, Guillaume C, Bea A, Arrayago MJ (1993) Interpretation biogeographique de la bimodalite de reproduction de lizard—Lacerta vivipara Jacquin—(Sauria, Lacertidae): un modele pour l’etude de l’evolution de la viviparite. Biogeographica 69:3–13
Heulin B, Ghielmi S, Vogrin N, Surget-Groba Y, Guillaume CP (2002) Variation in eggshell characteristics and in intrauterine egg retention between two oviparous clades of the lizard Lacerta vivipara: insight into the oviparity–viviparity continuum in squamates. J Morphol 252:255–262
Heulin B, Garnier D, Surget-Groba Y, Deunff J (2008) Plasma levels of estradiol during vitellogenesis and early gestation in oviparous and viviparous Lacerta (Zootoca) vivipara. Amphibia-Reptilia 29:135–139
Highfill DR, Mead RA (1975) Sources and levels of progesterone during pregnancy in the garter snake, Thamnophis elegans. Gen Comp Endocr 27:389–400
Higuchi R, Dollinger G, Walsh PS, Griffith R (1992) Simultaneous amplification and detection of specific DNA sequences. Biotechnology 10:413–417
Higuchi R, Fockler C, Dollinger G, Watson R (1993) Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology 11:1026–1030
Holmes KM, Cree A (2006) Annual reproduction in females of a viviparous skink (Oligosoma maccanni) in a subalpine environment. J Herpetol 40:141–151
Hoyer PE, Andersen H (1977) Histochemistry of 3β-hydroxysteroid dehydrogenase in rat ovary. Histochemistry 51:167–193
Huddleston H, Schust DJ (2004) Immune interactions at the maternal-fetal interfacte: a focus on antigen presentation. Am J Reprod Immunol 51:283–289
Hyland RA, Shaw TJ, Png FY, Murphy CR (1998) Pan-cadherin concentrates apically in uterine epithelial cells during uterine closure in the rat. Acta Histochem 100:75–81
Illingworth IM, Kiszka I, Bagley S, Ireland GW, Garrod DR, Kimber SJ (2000) Desmosomes are reduced in the mouse uterine luminal epithelium during the preimplantation period of pregnancy: a mechanism for facilitation of implantation. Biol Reprod 63:1764–1773
Janes DR, Organ CL, Fujita MK, Shedlock AM, Edwards SV (2010) Genome evolution in Reptilia, the sister group of mammals. Ann Rev Genom Hum Genet 11:239–264
Jenner RA, Wills MA (2007) The choice of model organisms in evo-devo. Nat Rev Genet 8:311–319
Jerez A, Ramírez-Pinilla MP (2003) Morphogenesis of extraembryonic membranes and placentation in Mabuya mabouya (Squamata, Scincidae). J Morphol 258:158–178
Jessop TS, Chan R, Stuart-Fox D (2009) Sex steroid correlates of female-specific colouration, behaviour and reproductive state in Lake Eyre dragon lizards, Ctenophorus maculosus. J Comp Physiol A 195:619–630
Jones RE, Guillette LJ (1982) Hormonal control of oviposition and parturition in lizards. Herpetologica 38:80–93
Jones RE, Guillette LJ, Summers CH, Tokarz RR, Crews D (1983) The relationship among ovarian condition, steroid hormones, and estrous behaviour in Anolis carolinensis. J Exp Zool 227:145–154
Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-β superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232
Jones SM, Swain R (1996) Annual reproductive cycle and annual cycles of reproductive hormones in plasma of female Niveoscincus metallicus (Scincidae) from Tasmania. J Herpetol 30:140–146
Jones SM, Wapstra E, Swain R (1997) Asynchronous male and female gonadal cycles and plasma steroid concentrations in a viviparous lizard, Niveoscincus ocellatus (Scincidae), from Tasmania. Gen Comp Endocr 108:271–281
Kaneda A, Takai D, Kaminishi M, Okochi E, Ushijima T (2003) Methylation-sensitive representational difference analysis and its application to cancer research. Ann New York Acad Sci 983:131–141
Katsu Y, Matsubara K, Kohno S, Matsuda Y, Toriba M, Oka K, Guillette LJ, Ohta Y, Iguchi T (2010) Molecular cloning, characterisation, and chromosome mapping of reptilian estrogen receptors. Endocrinology 0:en.2010-0356v1
Klein J (1986) The natural history of the major histocompatibility complex. Wiley, New York
Kleis-San Francisco SK, Callard IP (1986) Progesterone receptors in the oviduct of a viviparous snake (Nerodia): correlations with ovarian function and plasma steroid levels. Gen Comp Endocr 63:220–229
Khambaty M, Stewart JR, Ecay TW (2008) Developmental expression of carbonic anhydrase II in the extraembryonic membranes of the corn snake, Pantherophis guttatus. FASEB J 22:757.21
Kumazawa Y (2007) Mitochondrial genomes from major lizard families suggest their phylogenetic relationships and ancient radiations. Gene 388:19–26
Laird PW (2010) Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 11:191–203
Lee JJ, Radice G, Perkins CP, Costantini F (1992) Identification and characterisation of a novel, evolutionarily conserved gene disrupted by the murine Hβ58 embryonic lethal transgene insertion. Development 115:277–288
Limatola D’Uva E, Gaia Monti M, Di Montefiano R (1997) Production of an oxytocin like substance by the subcommissural organ (SCO), related to the reproductive cycle in oviparous and viviparous reptiles. J Neuroendocr 9:655–662
Lin A, Yan WH, Xu HH, Gan MF, Cai JF, Zhu M, Zhou MY (2007) HLA-G expression in human ovarian carcinoma counteracts NK cell function. Ann Oncol 18:1804–1809
Lind CM (2009) The relationship between seasonal steroid hormone concentrations and the reproductive cycle in the northern pacific rattlesnake, Crotalus oreganus. Unpublished masters thesis. The Faculty of California Polytechnic State University
Lind CM, Husak JF, Eikenaar C, Moore IT, Taylor EN (2010) The relationship between plasma steroid hormone concentrations and the reproductive cycle in the northern pacific rattlesnake, Crotalus oreganus. Gen Comp Endocr 166:590–599
Lindsay LA, Murphy CR (2007) Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat. J Mol Histol 38:87–95
Lisitsyn N, Lisitsyn N, Wigler M (1993) Cloning the differences between two complex genomes. Science 259:946–951
Liu H, Wintour EM (2005) Aquaporins in development—a review. Reprod Biol Endocr 3:18
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408
Losos J, Braun E, Brown D, Clifton S, Edwards S, Gibson-Brown J, Glenn T, Guillette L, Main D, Minx P, Modi W, Pfrender M, Pollock D, Ray D, Shedlock A, Warren W (2005) Proposal to sequence the first reptilian genome: the green anole lizard, Anolis carolinensis. NHGRI White Paper
Lovern MB, Wade J (2001) Maternal plasma and egg yolk testosterone concentrations during embryonic development in green anoles (Anolis carolinensis). Gen Comp Endocr 124:226–235
Lovern MB, Wade J (2003) Sex steroids in green anoles (Anolis carolinensis): uncoupled maternal plasma and yolking follicle concentrations, potential embryonic steroidogenesis, and evolutionary implications. Gen Comp Endocr 134:109–115
Lutterschmidt WI, Lutterschmidt DI, Mason RT, Reinert HK (2009) Seasonal variation in hormonal responses of timber rattlesnakes (Crotalus horridus) to reproductive and environmental stressors. J Comp Physiol B 179:747–757
MacDonald EA, Czekala NM, Berger GP, Alberts AC (2007) Diurnal and seasonal patterns in corticosterone in the turks and caicos iguana (Cyclura carinata carinata). Carrib J Sci 43:266–272
Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotech 21:255–261
Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141
Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517
Martinez-Torres M, Hernandez-Caballero ME, Alvarez-Rodriguez C, Luis-Diaz JA, Ortiz-Lopez G (2003) Luteal development and progesterone levels during pregnancy of the viviparous temperate lizard Barisia imbricata imbricata (Reptilia: Anguidae). Gen Comp Endocr 132:55–65
Masson GR, Guillette LJ (1987) Changes in oviducal vascularity during the reproductive cycle of three oviparous lizards (Eumeces obsoletus, Sceloporus undulatus and Crotaphytus collaris). J Reprod Fertil 80:361–371
Medawar PB (1953) Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp Soc Exp Biol 7:320–338
Mineur P, Colige AC, Deroanne CF, Dubail J, Kesteloot F, Habraken Y, Noel A, Voo S, Waltenberger J, Lapiere CM, Nusgens BV, Lambert CA (2007) Newly identified biologically active and proteolysis-resistant VEGF-A isoform VEGF 111 is induced by genotoxic agents. J Cell Biol 179:1261–1273
Moffett A, Loke C (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6:584–594
Moore MC, Whittier JM, Crews D (1985) Sex steroid hormones during the ovarian cycle of an all-female, parthenogenetic lizard and their correlation with pseudosexual behaviour. Gen Comp Endocr 60:144–153
Moore MC, Crews D (1986) Sex steroid hormones in natural populations of a sexual whiptail lizard Cnemidophorus inornatus, a direct evolutionary ancestor of a unisexual parthenogen. Gen Comp Endocr 63:424–430
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Method 5:621–628
Murphy BEP (1964) Application of the property of protein-binding to the assay of minute quantities of hormones and other substances. Nature 201:679
Murphy BF, Thompson MB, Belov K (2009) Evolution of viviparity and the maternal immune system: major histocompatibility complex (MHC) class I genes in skinks. Orbit 1:1–17
Murphy BF, Parker SL, Murphy CR, Thompson MB (2010a) Angiogenesis of the uterus and chorioallantois in the eastern water skink Eulamprus quoyii. J Exp Biol 213:3340–3347
Murphy BF, Belov K, Thompson MB (2010b) Evolution of viviparity and uterine angiogenesis: vascular endothelial growth factor (VEGF) in oviparous and viviparous skinks. J Exp Zool B 314:148–156
Murphy BF, Parker SL, Murphy CR, Thompson MB (2011) Placentation in the eastern water skink (Eulamprus quoyii): a placentome-like structure in a lecithotrophic lizard. J Anat. doi:10.1111/j.1469-7580.2011.01368.x
Naulleau G, Fleury F (1990) Changes in plasma progesterone in female Vipera aspis L. (Reptilia, Viperidae) during the sexual cycle in pregnant and nonpregnant females. Gen Comp Endocr 78:433–443
Packard GC, Tracey CR, Roth JJ (1977) The physiological ecology of reptilian eggs and embryos, and the evolution of viviparity within the class Reptilia. Biol Rev 52:71–105
Packard GC (1991) Physiological and ecological importance of water to embryos of oviparous reptiles. In: Deeming CD, Ferguson MWJ (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 213–228
Packard MJ, Packard GC, Gutzke WHN (1984) Calcium metabolism in embryos of the oviparous snake Coluber constrictor. J Exp Biol 110:99–112
Packard MJ, Packard GC, Miller JD, Jones ME, Gutzke WHN (1985) Calcium mobilization, water balance, and growth in embryos of the agamid lizard Amphibolurus barbatus. J Exp Zool 235:349–357
Painter D, Jennings DH, Moore MC (2002) Placental buffering of maternal steroid hormone effects on fetal and yolk hormone levels: a comparative study of a viviparous lizard, Sceloporus jarrovi, and an oviparous lizard, Sceloporus graciosus. Gen Comp Endocr 127:105–116
Painter DL, Moore MC (2005) Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal-fetal hormone exchange. Physiol Biochem Zool 78:364–372
Palmer BD, DeMarco VG, Guillette LJ Jr (1993) Oviductal morphology and eggshell formation in the lizard Sceloporus woodi. J Morphol 217:205–217
Pang CNI, Gasteiger E, Wilkins MR (2010) Identification of arginine- and lysine-methylation in the proteome of Saccharomyces cerevisiae and its functional implications. BMC Genom 11:92
Paolucci M, Di Cristo C (2002) Progesterone receptor in the liver and oviduct of the lizard Podarcis sicula. Life Sci 71:1417–1427
Paria BC, Reese J, Das SK, Dey SK (2002) Deciphering the cross-talk of implantation: advances and challenges. Science 296:2185
Parker SL, Manconi F, Murphy CR, Thompson MB (2010) Uterine and placental angiogenesis in the Australian skinks, Ctenotus taeniolatus and Saiphos equalis. Anat Rec 293:829–838
Paulesu L (1997) Cytokines in mammalian reproduction and speculation about their possible involvement in nonmammalian viviparity. Microsc Res Techniq 38:188–194
Paulesu L, Romagnoli R, Marchetti M, Cintorino M, Ghiara P, Guarino FM, Ghiara G (1995) Cytokines in the viviparous reproduction of squamate reptiles: Interleukin-1α (IL-1α) and IL-1β in placental structures of a skink. Placenta 16:193–205
Paulesu L, Cateni C, Romagnoli R, Chellini F, Angelini F, Guarino FM, Rider V, Imakawa K, Bigliardi E (2001) Evidence of Hβ58, a gene involved in mammalian placental development, in the three-toed skink, Chalcides chalcides (Squamata: Scincidae), a viviparous placentotrophic reptile. Placenta 22:735–741
Paulesu L, Romagnoli R, Bigliardi E (2005a) Materno-fetal immunotolerance: is interleukin-1 a fundamental mediator in placental viviparity? Dev Comp Immunol 29:409–415
Paulesu L, Bigliardi E, Paccagnini E, Ietta F, Cateni C, Guillaume CP, Heulin B (2005b) Cytokines in the oviparity/viviparity transition: Evidence of the interleukin-1 system in a species with reproductive bimodality, the lizard Lacerta vivipara. Evol Dev 7:282–288
Petroff MG (2005) Immune interactions at the maternal-fetal interface. J Reprod Immunol 68:1–13
Phillips JA, Millar RP (1998) Reproductive biology of the white-throated savanna monitor, Varanus albigularis. J Herpetol 32:366–377
Pijnenborg R, Robertson WB, Brosens I, Dixon G (1981) Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2:71–92
Polzonetti-Magni A, Facchinetti F, Carnevali O, Mosconi G, Pestarino M, Vallarino M, Ciarcia G (1994) Presence and steroidogenic activity of β-endorphin in the ovary of the lizard, Podarcis s. sicula Raf. Biol Reprod 50:1059–1065
Qualls CP (1997) The effects of reproductive mode and climate on reproductive success in the Australian lizard, Lerista bougainvillii. J Herpetol 31:60–65
Qualls CP, Shine R, Donnellan S, Hutchinson M (1995) The evolution of viviparity within the Australian scincid lizard Lerista bougainvillii. J Zool Lond 237:13–26
Radder RS, Shanbhag BA, Saidapur SK (2001) Pattern of sex steroid hormone level during reproductive cycles of male and female tropical lizard, Calotes versicolor. Gen Comp Endocr 124:285–292
Radice G, Lee JJ, Costantini F (1991) Hβ58, and insertional mutation effecting early postimplantation development of the mouse embryo. Development 111:801–811
Ramirez-Pinilla MP (2006) Placental transfer of nutrients during gestation in an Andean population of the highly matrotrophic lizard genus Mabuya (Squamata: Scincidae). Herpetol Monogr 20:194–204
Rhen T, Sakata JT, Zeller M, Crews D (2000) Sex steroid levels across the reproductive cycle of female leopard geckos, Eublepharis macularius, from different incubation temperatures. Gen Comp Endocr 118:322–331
Rhen T, Crews D (2001) Distribution of androgen and estrogen receptor mRNA in the brain and reproductive tissues of the leopard gecko, Eublepharis macularius. J Comp Neurol 437:385–397
Rhen T, Sakata JT, Woolley S, Porter R, Crews D (2003) Changes in androgen receptor mRNA expression in the forebrain and oviduct during the reproductive cycle of female leopard geckos, Eublepharis macularius. Gen Comp Endocr 132:133–141
Richards RG, DiAugustine RP, Petrusz P, Clark GC, Sebastian J (1996) Estradiol stimulates tyrosine phosphorylation of the insulin-like growth factor-1 receptor and insulin receptor substrate-1 in the uterus. Proc Natl Acad Sci USA 93:12002–12007
Rider V, Jones SR, Foster RT, Imakawa K (2000) Changes in the temporal and spatial expression of Hβ58 during formation and maturation of the chorioallantoic placenta in the rat. Biol Reprod 63:1735–1746
Riley D, Kleis-San Francisco SM, Callard IP (1988) A plasma steroid hormone binding protein in the viviparous water snake Nerodia. Gen Comp Endocr 71:419–428
Robertson WR (1979) A quantitative cytochemical method for the demonstration of Δ5, 3β-hydroxysteroid dehydrogenase activity in unfixed tissue sections of rat ovary. Histochemistry 59:271–285
Rokas A, Abbot P (2009) Harnessing genomics for evolutionary insights. Trends Ecol Evol 24:192–200
Romagnoli R, Cateni C, Guarino FM, Bigliardi E, Paulesu LR (2003) Potential role of interleukin-1 at the peri-ovulation stage in a species of placental viviparous reptile, the three-toed skink, Chalcides chalcides (Squamata: Scincidae). Reprod Biol Endocr 1:60–65
Rubenstein DR, Wikelski M (2005) Steroid hormones and aggression in female Galapagos marine iguanas. Horm Behav 48:329–341
Saito S (2001) Cytokine cross-talk between mother and the embryo/placenta. J Reprod Immunol 52:15–33
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Nat Acad Sci USA 74:5463–5467
Schafer-Somi S (2003) Cytokines during early pregnancy of mammals: a review. Anim Reprod Sci 75:73–94
Schuett GW, Grober MS, Van Kirk EA, Murdoch WJ (2004) Long-term sperm storage and plasma steroid profile of pregnancy in a western diamond-backed rattlesnake (Crotalus atrox). Herpetol Rev 35:328–333
Schwartz TS, Tae H, Yang Y, Mockaitis K, Van Hemert JL, Proulx SR, Choi JH, Bronikowski AM (2010) A garter snake transcriptome: pyrosequencing, de novo assembly, and sex-specific differences. BMC Genom 11:694
Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, Borg C, Saas P, Tiberghien P, Rouas-Friess N, Carosella ED, Deschaseaux F (2008) HLA-G5 secretion by human mesenchymal stem cells is required to suppress T-lymphocyte and NK function and to induce CD4 + CD25highFOXP3 + regulatory T cells. Stem Cells 26:212–222
Shanbhag BA, Radder RS, Saidapur SK (2001) Plasma progesterone levels and luteal activity during gestation and prolonged oviductal egg retention in a tropical lizard, Calotes versicolor. Gen Comp Endocr 123:73–79
Simon C, Frances A, Piquette GN, Danasouri IE, Zurawski G, Dang W, Polan ML (1994) Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 134:521–528
Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15:342–355
Sindelka R, Ferjentsik Z, Jonak J (2006) Developmental expression profiles of Xenopus laevis reference genes. Dev Dynam 235:754–758
Singh P, Krishna A, Sridaran R (2007) Localisation of gonadotrophin-releasing hormone I, bradykinin and their receptors in the ovaries of non-mammalian vertebrates. Reproduction 133:969–981
Singh P, Krishna A, Sridaran R, Tsutsui K (2008) Changes in GnRHI, bradykinin and their receptors and GnIH in the ovary of Calotes versicolor during reproductive cycle. Gen Comp Endocr 159:158–169
Smith SA, Shine R (1997) Intraspecific variation in reproductive mode within the scincid lizard Saiphos equalis. Aust J Zool 45:435–445
Snell GD (1981) Studies in histocompatibility. Science 213:172–178
Sparkman AM, Vleck CM, Bronikowski AM (2009) Evolutionary ecology of endocrine-mediated life-history variation in the garter snake Thamnophis elegans. Ecology 90:720–728
Sparkman AM, Byars D, Ford NB, Bronikowski AM (2010) The role of insulin-like growth factor-1 (IGF-1) in growth and reproduction in female brown house snakes (Lamprophis fuliginosus). Gen Comp Endocr 168:408–414
Stewart JR, Ecay TW (2010) Patterns of maternal provision and embryonic mobilization of calcium in oviparous and viviparous squamate reptiles. Herpetol Conserv Biol 5(2)
Stewart JR, Mathieson AN, Ecay TW, Herbert JF, Parker SL, Thompson MB (2010a) Uterine and eggshell structure and histochemical in a lizard with prolonged uterine egg retention (Lacertilia, Scincidae, Saiphos). J Morphol 271:1342–1351
Stewart JR, Thompson MB (1994) Placental structure of the Australian lizard, Niveoscincus metallicus (Squamata: Scincidae). J Morphol 220:223–236
Stewart JR, Thompson MB (1996) Extraembryonic membranes of the Australian scincid lizards Bassiana duperreyi (oviparous) and Pseudemoia entrecasteauxii (viviparous). J Morphol 227:349–370
Stewart JR, Thompson MB (2000) Evolution of placentation among squamate reptiles: recent research and future directions. Comp Biochem Physiol A 127:411–431
Stewart JR, Thompson MB (2009) Placental ontogeny in Tasmanian snow skinks (Genus Niveoscnicus) (Lacertilia: Scincidae). J Morphol 270:485–516
Stewart JR, Mathieson AN, Ecay TW, Herbert JF, Parker SL, Thompson MB (2010b) Uterine and eggshell structure and histochemical in a lizard with prolonged uterine egg retention (Lacertilia, Scincidae, Saiphos). J Morphol 271:1342–1351
Stroynowski I, Lindahl KF (1994) Antigen presentation by non-classical class I molecules. Curr Opin Immunol 6:38–44
Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, Schmidt D, O’Keeffe S, Haas S, Vingron M, Lehrach H, Yaspo M (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321:956–960
Takeichi M (1990) Cadherins: a molecular family important in selective cell-cell adhesion. Ann Rev Biochem 59:237–252
Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch BB, Siddiqui A, Lao K, Surani MA (2009) mRNA-Seq whole transcriptome analysis of a single cell. Nat Methods 6:377–382
Tang R, Dodd A, Lai D, McNabb WC, Love DR (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalisation. Acta Bioch Bioph Sin 39:384–390
Taylor EN, DeNardo DF, Jennings DH (2004) Seasonal steroid hormone levels and their relation to reproduction in the western diamond-backed rattlesnake, Crotalus atrox (Serpentes: Viperidae). Gen Comp Endocr 136:328–337
Taylor HS, Vanden Heuvel GB, Igarashi P (1997) A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the HOXA cluster genes. Biol Reprod 57:1338–1345
Thompson J (1977) Embryo-Maternal Relationships in a Viviparous Lizard, Sphenomorphus quoyii (Dumeril and Bibron). Unpublished PhD dissertation
Thompson J (1981) A study of the sources of nutrients for embryonic development in a viviparous lizard, Sphenomorphus quoyii. Comp Biochem Physiol A 70:509–518
Thompson MB, Speake BK (2006) A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. J Comp Physiol B 176:179–189
Thompson MB, Stewart JR, Speake BK (2000) Comparison of nutrient transport across the placenta of lizards differing in placental complexity. Comp Biochem Physiol A 127:469–479
Thompson MB, Stewart JR, Speake BK, Hosie MJ, Murphy CR (2002) Evolution of viviparity: what can Australian lizards tell us? Comp Biochem Physiol B 131:631–643
Thompson MB, Lindsay LA, Herbert JF, Murphy CR (2007) Calcium ATPase expression in the oviducts of the skink, Lampropholis guichenoti. Comp Biochem Physiol A 147:1090–1094
Thomson M, Herbert JF, Murphy CR, Thompson MB (2005) HoxA10-like proteins in the reproductive tract of the viviparous lizard Eulamprus tympanum and the oviparous lizard Lampropholis guichenoti. Comp Biochem Physiol B 142:123–127
Thomson M, Herbert JF, Thompson MB (2006) Tyrosine phosphorylated proteins in the reproductive tract of the viviparous lizard Eulamprus tympanum and the oviparous lizard Lampropholis guichenoti. Comp Biochem Physiol B 144:382–386
Tokarz RR, Crews D, McEwen BS (1981) Estrogen-sensitive progestin binding sites in the brain and oviduct of the lizard, Anolis carolinensis. Brain Res 22:95–105
Tousignant A, Viets B, Flores D, Crews D (1995) Ontogenetic and social factors affect the endocrinology and timing of reproduction in the female leopard gecko (Eublepharus macularis). Horm Behav 29:141–153
Toyota M, Ho C, Ahuja N, Jair K, Li Q, Ohe-Toyota M, Baylin SB, Issa JJ (1999) Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res 59:2307–2312
Trowsdale J, Betz AG (2006) Mother’s little helpers: mechanisms of maternal-fetal tolerance. Nat Immunol 7:241–246
Tsai TS, Tu MC (2001) Reproductive cycle of female chinese green tree vipers, Trimeresurus stejnegeri stejnegeri, in Northern Taiwan. Herpetologica 57:157–168
Van Itallie CM, Anderson JM (2006) Claudins and epithelial paracellular transport. Ann Rev Physiol 68:403–429
van Wyk JH (1994) Physiological changes during the female reproductive cycle of the viviparous lizard Cordylus giganteus (Sauria: Cordylidae). Herpetologica 50:480–493
Veith WJ (1974) Reproductive biology of Chamaeleo pumilus pumilus with specific reference to the role of the corpus luteum and progesterone. Zool Afr 9:161–183
Vieira S, de Perez G, Ramirez-Pinilla MP (2007) Invasive cells in the placentome of Andean populations of Mabuya: An endotheliochorial contribution to the placenta. Anat Rec 290:1508–1518
Vigano P, Mangioni S, Pompei F, Chiodo I (2003) Maternal-conceptus cross talk–a review. Placenta 24:S56–S61
Wack CL, Fox SF, Hellgren EC, Lovern MB (2008) Effects of sex, age, and season on plasma steroids in free-ranging Texas horned lizards (Phrynosoma cornutum). Gen Comp Endocr 155:589–596
Wall CE, Cozza S, Riquelme CA, McCombie WR, Heimiller JK, Marr TG, Leinward LA (2011) Whole transcriptome analysis of the fasting and fed Burmese python heart: Insights into extreme physiological cardiac adaptation. Physiol Genom 43:69–79
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63
Weekes HC (1929) On placentation in reptiles I. Proc Linn Soc New South Wales 54:34–60
Weekes HC (1930) On placentation in reptiles II. Proc Linn Soc New South Wales 55:550–576
Weekes HC (1935) A review of placentation among reptiles with particular regard to the function and evolution of the placenta. Proc Zool Soc Lond 1935:625–645
Weiss SL, Jennings DH, Moore MC (2002) Effect of captivity in semi-natural enclosures on the reproductive endocrinology of female lizards. Gen Comp Endocr 128:238–246
Whittier JM, Mason RT, Crews D (1987) Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: relationship to mating and gestation. Gen Comp Endocr 67:33–43
Whittier JM, West NB, Brenner RM (1991) Immunorecognition of estrogen receptors by monoclonal antibody H222 in reproductive tissues of the red-sided garter snake. Gen Comp Endocr 81:1–6
Wilhelm BT, Landry JR (2009) RNA-Seq-quantitative measurement of expression through massively parallel RNA-sequencing. Methods 48:249–257
Wilson BS, Wingfield JC (1992) Correlation between female reproductive condition and plasma corticosterone in the lizard Uta stansburiana. Copeia 1992:691–697
Wilson BS, Wingfield JC (1994) Seasonal and interpopulational variation in plasma levels of corticosterone in the side-blotched lizard (Uta stansburiana). Physiol Zool 67:1025–1049
Wittwer CT, Herrmann MG, Moss AA, Rasmussen RP (1997) Continuous fluorescence monitoring of rapid cycle DNA amplification. Biotechniques 22:130–138
Wooding FBP, Ramirez-Pinilla MP, Forhead AS (2010) Functional studies of the placenta of the lizard Mabuya sp. (Scincidae) using immunocytochemistry. Placenta 31:675–685
Woodley SK, Moore MC (1998) Female territorial aggression and steroid hormones in mountain spiny lizards. Anim Behav 57:1083–1089
Woodley SK, Moore MC (2002) Plasma corticosterone response to an acute stressor varies according to reproductive condition in female tree lizards (Urosaurus ornatus). Gen Comp Endocr 128:143–148
Wu Q, Thompson MB, Murphy CR (2011) Changing distribution of cadherins during gestation in the uterine epithelium of lizards. J Exp Zool (in press)
Xavier F (1982) Progesterone in the viviparous lizard Lacerta vivipara: Ovarian biosynthesis, plasma levels, and binding to transcortin-type protein during the sexual cycle. Herpetologica 38:62–70
Young LJ, Godwin J, Grammer M, Gahr M, Crews D (1995a) Reptilian sex steroid receptors: amplification, sequence and expression analysis. J Steroid Biochem 55:261–269
Young LJ, Nag PK, Crews D (1995b) Species differences in estrogen receptor and progesterone receptor-mRNA expression in the brain of sexual and unisexual whiptail lizards. J Neuroendocr 7:567–576
Zhao X, Leon IR, Bak S, Mogensen M, Brzezinski K, Højlund K, Jensen ON (2011) Phosphoproteome analysis of functional mitochondria isolated from resting human muscle reveals extensive phosphorylation of inner membrane protein complexes and enzymes. Mol Cell Proteomics 10:1–14
Zourbas S, Dubanchet S, Martal J, Chaouat G (2001) Localisation of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetal-maternal interface during murine pregnancy. Clin Exp Immunol 126:519–528
Acknowledgments
This review and the ideas it contains was supported by ARC Discovery grants to MBT and C. R. Murphy. We wish to thank M. C. Brandley and S. L. Parker for helpful discussions of ideas in this manuscript.
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Murphy, B.F., Thompson, M.B. A review of the evolution of viviparity in squamate reptiles: the past, present and future role of molecular biology and genomics. J Comp Physiol B 181, 575–594 (2011). https://doi.org/10.1007/s00360-011-0584-0
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DOI: https://doi.org/10.1007/s00360-011-0584-0