How organs originate and evolve is a question fundamental to understanding the evolution of complex multicellular life forms. Vertebrates have a relatively standard body plan with more or less the same conserved set of organs. The placenta is a comparatively more recently evolved organ, derived in many lineages independently. Using placentas as a model, we discuss the genetic basis for organ origins. We show that the evolution of placentas occurs by acquiring new functional attributes to existing tissues, changes in the patterning and development of tissues, and the evolution of novel cell types. We argue that a diversity of genomic changes facilitated these physiological transformations and that these changes are likely to have occurred during the evolution of organs more broadly. Finally, we argue that a key aspect to understanding the evolutionary origin of organs is that they are likely to result from novel interactions between distinct cell populations.
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The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish
BMC Evolutionary Biology Open Access 26 July 2019
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Oakley, T. H. & Speiser, D. I. How complexity originates: the evolution of animal eyes. Annu. Rev. Ecol. Evol. Syst. 46, 237–260 (2015).
Gregory, T. R. The evolution of complex organs. Evo. Edu. Outreach 1, 358–389 (2008).
Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).
Mossman, H. Comparative Morphogenesis of the Fetal Membranes and Accessory Uterine Structures Vol. 26 (Carnegie Institution of Washington, 1937).
Van Dyke, J. U., Brandley, M. C. & Thompson, M. B. The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes. Reproduction 147, R15–R26 (2014).
Reznick, D. N., Mateos, M. & Springer, M. S. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298, 1018–1020 (2002).
Blackburn, D. G. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J. Morphol. 276, 961–990 (2015).
Stewart, J. R. Placental specializations in lecithotrophic viviparous squamate reptiles. J. Exp. Zool. Part B 324, 549–561 (2015).
Wright, A. M., Lyons, K. M., Brandley, M. C. & Hillis, D. M. Which came first: the lizard or the egg? Robustness in phylogenetic reconstruction of ancestral states. J. Exp. Zool. Part B 324, 504–516 (2015).
Griffith, O. W. et al. 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 (2015).
Cornetti, L., Ficetola, G. F., Hoban, S. & Vernesi, C. Genetic and ecological data reveal species boundaries between viviparous and oviparous lizard lineages. Heredity 115, 517–526 (2015).
Murphy, B. & Thompson, M. 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 181B, 575–594 (2011).
Brigandt, I. & Love, A. C. Conceptualizing evolutionary novelty: moving beyond definitional debates. J. Exp. Zool. Part B 318, 417–427 (2012).
Müller, G. B. & Wagner, G. P. Novelty in evolution: restructuring the concept. Annu. Rev. Ecol. Syst. 22, 229–256 (1991).
Wagner, G. P. Evolutionary innovations and novelties: let us get down to business! Zool. Anz. 256, 75–81 (2015).
Love, A. C. Evolutionary morphology, innovation, and the synthesis of evolutionary and developmental biology. Biol. Philos. 18, 309–345 (2003).
Wagner, G. P. Homology, Genes and Evolutionary Innovation (Princeton Univ. Press, 2014).
Arendt, D. et al. Evolution of sister cell types by individuation. Nat. Rev. Genet. 17, 744–757 (2016).
Wagner, G. P., Pavlicev, M. & Cheverud, J. M. The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).
Eddy, S. R. The C-value paradox, junk DNA and ENCODE. Curr. Biol. 22, R898–R899 (2012).
Richter, D. J. & King, N. The genomic and cellular foundations of animal origins. Annu. Rev. Genet. 47, 509–537 (2013).
Erwin, D. H. Early origin of the bilaterian developmental toolkit. Phil. Trans. R. Soc. B 364, 2253–2261 (2009).
Chen, S., Krinsky, B. H. & Long, M. New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 14, 645–660 (2013).
Blackburn, D. G. Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J. Exp. Zool. 282, 560–617 (1998).
Thompson, M. B. & Speake, B. K. A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. J. Comp. Physiol. 176B 179–189 (2006).
Cruze, L., Hamlin, H. J., Kohno, S., McCoy, M. W. & Guillette Jr, L. J. Evidence of steroid hormone activity in the chorioallantoic membrane of a Turtle (Pseudemys nelsoni). Gen. Comp. Endocr. 186, 50–57 (2013).
Griffith, O. W., Brandley, M. C., Whittington, C. M., Belov, K. & Thompson, M. B. Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes. Gen. Comp. Endocrinol. http://dx.doi.org/10.1016/j.ygcen.2016.04.017 (2016).
Linville, B. et al. Placental calcium provision in a lizard with prolonged oviductal egg retention. J. Comp. Physiol. B 180B 221–227 (2010).
Herbert, J. F., Murphy, C. R. & Thompson, M. B. Calcium ATPase localization in the uterus of two species of Pseudemoia (Lacertilia: Scincidae) with complex placentae. Herpetol. Conserv. Biol. 5, 290–296 (2010).
Stewart, J. R., Ecay, T. W., Heulin, B., Fregoso, S. P. & Linville, B. J. Developmental expression of calcium transport proteins in extraembryonic membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae). J. Exp. Biol. 214, 2999–3004 (2011).
Blank, D., Wolf, L., Ackermann, M. & Silander, O. K. The predictability of molecular evolution during functional innovation. Proc. Natl Acad. Sci. USA 111, 3044–3049 (2014).
Dennis, A. B., Dunning, L. T., Sinclair, B. J. & Buckley, T. R. Parallel molecular routes to cold adaptation in eight genera of New Zealand stick insects. Sci. Rep. 5, 13965 (2015).
Rawn, S. M. & Cross, J. C. The evolution, regulation, and function of placenta-specific genes. Annu. Rev. Cell Dev. Biol. 24, 159–181 (2008).
Schep, R. et al. Control of Hoxd gene transcription in the mammary bud by hijacking a preexisting regulatory landscape. Proc. Natl Acad. Sci. USA 113, E7720–E7729 (2016).
Lynch, V. J. et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 10, 551–561 (2015).
Griffith, O. W., Brandley, M. C., Belov, K. & Thompson, M. B. Reptile pregnancy is underpinned by complex changes in uterine gene expression: a comparative analysis of the uterine transcriptome in viviparous and oviparous lizards. Genome Biol. Evol. 8, 3226–3239 (2016).
Kin, K. et al. The transcriptomic evolution of mammalian pregnancy: gene expression innovations in endometrial stromal fibroblasts. Genome Biol. Evol. 8, 2459–2473 (2016).
Wittkopp, P. J. & Kalay, G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13, 59–69 (2012).
Carter, A. M. Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol. Rev. 92, 1543–1576 (2012).
Lowdon, R. F., Jang, H. S. & Wang, T. Evolution of epigenetic regulation in vertebrate genomes. Trends Genet. 32, 269–283 (2016).
Feschotte, C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397–405 (2008).
Emera, D. et al. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29, 239–247 (2012).
Chuong, E. B., Rumi, M. A. K., Soares, M. J. & Baker, J. C. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45, 325–329 (2013).
Lynch, V. J., Leclerc, R. D., May, G. & Wagner, G. P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43, 1154–1158 (2011).
Kordis, D. Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet. Genome Res. 127, 94–111 (2009).
Gilbert, C., Hernandez, S. S., Flores-Benabib, J., Smith, E. N. & Feschotte, C. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol. Biol. Evol. 29, 503–515 (2011).
Whittington, C. M., Griffith, O. W., Qi, W., Thompson, M. B. & Wilson, A. B. Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. Mol. Biol. Evol. 32, 3114–3131 (2015).
Fried, C., Prohaska, S. J. & Stadler, P. F. Exclusion of repetitive DNA elements from gnathostome Hox clusters. J. Exp. Zool. Part B 302B 165–173 (2004).
Di-Poï, N. et al. Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464, 99–103 (2010).
Long, M., VanKuren, N. W., Chen, S. & Vibranovski, M. D. New gene evolution: little did we know. Annu. Rev. Genet. 47, 307–333 (2013).
Knox, K. & Baker, J. C. Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res. 18, 695–705 (2008).
Zhang, J. Z. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292–298 (2003).
Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).
Varanou, A. et al. The importance of cysteine cathepsin proteases for placental development. J. Mol. Med. 84, 305–317 (2006).
Puente, X. S. & López-Otín, C. A genomic analysis of rat proteases and protease inhibitors. Genome Res. 14, 609–622 (2004).
Ramsey, E. M. The Placenta Human and Animal (Praeger, 1982).
Gundling, W. E. & Wildman, D. E. A review of inter- and intraspecific variation in the eutherian placenta. Phil. Trans. R. Soc. B 370, 20140072 (2015).
Blackburn, D. G., Avanzati, A. M. & Paulesu, L. Classics revisited. History of reptile placentology: Studiati's early account of placentation in a viviparous lizard. Placenta 36, 1207–1211 (2015).
Carter, A. M. & Enders, A. C. Placentation in mammals: definitive placenta, yolk sac and paraplacenta. Theriogenology 86, 278–287 (2016).
Stölting, K. N. & Wilson, A. B. Male pregnancy in seahorses and pipefish: beyond the mammalian model. BioEssays 29, 884–896 (2007).
Ripley, J. L. Osmoregulatory role of the paternal brood pouch for two Syngnathus species. Comp. Biochem. Physiol. Part A 154, 98–104 (2009).
Carcupino, M., Baldacci, A., Mazzini, M. & Franzoi, P. Functional significance of the male brood pouch in the reproductive strategies of pipefishes and seahorses: a morphological and ultrastructural comparative study on three anatomically different pouches. J. Fish Biol. 61, 1465–1480 (2002).
Fiedler, K. Hormonale auslösung der geburtsbewegungen beim seepferdchen (Hippocampus, Syngnathidae, Teleostei). Z. Tierpsychol. 27, 679–686 (1970).
Shubin, N., Tabin, C. & Carroll, S. Deep homology and the origins of evolutionary novelty. Nature 457, 818–823 (2009).
Wagner, G. P. & Lynch, V. J. Evolutionary novelties. Curr. Biol. 20, R48–R52 (2010).
Arendt, D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868–882 (2008).
Wagner, G. P. What is “homology thinking” and what is it for? J. Exp. Zool. Part B 326, 3–8 (2015).
Liang, C., the, F. C., Forrest, A. R. R. & Wagner, G. P. The statistical geometry of transcriptome divergence in cell-type evolution and cancer. Nat. Commun. 6, 6066 (2015).
Chavan, A. R., Bhullar, B. A. & Wagner, G. P. What was the ancestral function of decidual stromal cells? A model for the evolution of eutherian pregnancy. Placenta 40, 40–51 (2016).
Kin, K., Nnamani, Mauris C., Lynch, Vincent J., Michaelides, E. & Wagner, Günter P. Cell-type phylogenetics and the origin of endometrial stromal cells. Cell Rep. 10, 1398–1409 (2015).
Kin, K., Maziarz, J. & Wagner, G. P. Immunohistological study of the endometrial stromal fibroblasts in the opossum, Monodelphis domestica: evidence for homology with eutherian stromal fibroblasts. Biol. Reprod. 90, 111 (2014).
Vasquez, Y. M. et al. FOXO1 is required for binding of PR on IRF4, novel transcriptional regulator of endometrial stromal decidualization. Mol. Endocrinol. 29, 421–433 (2015).
Nnamani, Mauris C. et al. A derived allosteric switch underlies the evolution of conditional cooperativity between HOXA11 and FOXO1. Cell Rep. 15, 2097–2108 (2016).
Small, C. M., Harlin-Cognato, A. D. & Jones, A. G. Functional similarity and molecular divergence of a novel reproductive transcriptome in two male-pregnant Syngnathus pipefish species. Ecol. Evol. 3, 4092–4108 (2013).
Sonderegger, S., Pollheimer, J. & Knöfler, M. Wnt signalling in implantation, decidualisation and placental differentiation — review. Placenta 31, 839–847 (2010).
Hill, J. A. Maternal–embryonic cross-talk. Ann. NY Acad. Sci. 943, 17–25 (2001).
Guzeloglu-Kayisli, O., Kayisli, U. A. & Taylor, H. S. The role of growth factors and cytokines during implantation: endocrine and paracrine interactions. Semin. Reprod. Med. 27, 062–079 (2009).
Fritz, R. R., Jain, C. & Armant, R. Cell signaling in trophoblast-uterine communication. Int. J. Dev. Biol. 58, 261–271 (2014).
Murphy, B. F., Parker, S. L., Murphy, C. R. & Thompson, M. B. Placentation in the eastern water skink (Eulamprus quoyii): a placentome-like structure in a lecithotrophic lizard. J. Anat. 218, 678–689 (2011).
Mor, G., Cardenas, I., Abrahams, V. & Guller, S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann. NY Acad. Sci. 1221, 80–87 (2011).
Brandley, M. C., Young, R. L., Warren, D. L., Thompson, M. B. & Wagner, G. P. 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 (2012).
Schlosser, G. in International Review of Cell and Molecular Biology Vol. 283 (ed. Kwang, J. ) 129–234 (Academic, 2010).
Gilbert, S. F. & Barresi, M. J. F. Developmental Biology 10th edn (Sinaur Associates, 2016).
Chen, C.-F. et al. Development, regeneration, and evolution of feathers. Annu. Rev. Anim. Biosci. 3, 169–195 (2015).
Marcotte, M., Sharma, R. & Bouchard, M. Gene regulatory network of renal primordium development. Pediatr. Nephrol. 29, 637–644 (2014).
Le Guen, L., Marchal, S., Faure, S. & de Santa Barbara, P. Mesenchymal–epithelial interactions during digestive tract development and epithelial stem cell regeneration. Cell Mol. Life Sci. 72, 3883–3896 (2015).
Grove, B. D. & Wourms, J. P. The follicular placenta of the viviparous fish, Heterandria formosa. I. Ultrastructure and development of the embryonic absorptive surface. J. Morphol. 209, 265–284 (1991).
Dunn, C. W., Giribet, G., Edgecombe, G. D. & Hejnol, A. Animal phylogeny and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 45, 371–395 (2014).
Budd, G. E. Early animal evolution and the origins of nervous systems. Phil. Trans. R Soc. B 370, 20150037 (2015).
Telford, M. J., Budd, G. E. & Philippe, H. Phylogenomic insights into animal evolution. Curr. Biol. 25, R876–R887 (2015).
Jondelius, U., Ruiz-Trillo, I., Baguñà, J. & Riutort, M. The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool. Scripta. 31, 201–215 (2002).
Turner, C. L. Pseudoamnion, pseudochorion, and follicular pseudoplacenta in poeciliid fishes. J. Morphol. 67, 59–89 (1940).
Griffith, O. W., Brandley, M. C., Belov, K. & Thompson, M. B. Allelic expression of mammalian imprinted genes in a matrotrophic lizard, Pseudemoia entrecasteauxii. Dev. Genes Evol. 226, 79–85 (2016).
Li, H., Elphick, M. & Shine, R. Potential targets for selection during the evolution of viviparity in cold-climate reptiles. Oecologiahttp://dx.doi.org/10.1007/s00442-00016-03752-00449 (2016).
Wourms, J. P. & Lombardi, J. Reflections on the evolution of piscine viviparity. Am. Zoologist 32, 276 (1992).
Van Dyke, J. U., Griffith, O. W. & Thompson, M. B. High food abundance permits the evolution of placentotrophy: evidence from a placental lizard, Pseudemoia entrecasteauxii. Am. Nat. 184, 198–210 (2014).
Trexler, J. C. & DeAngelis, D. L. Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy. Am. Nat. 162, 574–585 (2003).
Crespi, B. & Semeniuk, C. Parent–offspring conflict in the evolution of vertebrate reproductive mode. Am. Nat. 163, 635–653 (2004).
Haig, D. Placental hormones, genomic imprinting, and maternal—fetal communication. J. Evol. Biol. 9, 357–380 (1996).
Garratt, M., Gaillard, J.-M., Brooks, R. C. & Lemaître, J.-F. Diversification of the eutherian placenta is associated with changes in the pace of life. Proc. Natl Acad. Sci. USA 110, 7760–7765 (2013).
This research was funded by the Gaylord Donnelley Postdoctoral Environmental Fellowship to O.W.G. and a John Templeton Foundation Grant to G.P.W. (no. 54860). The authors thank T. Stewart, E. Erckenbrack, A. Chavan, C. Laing and F. Stabile for useful comments on drafts of this manuscript and M. Thompson for his encouragement to write it.
The authors declare no competing financial interests.
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Griffith, O., Wagner, G. The placenta as a model for understanding the origin and evolution of vertebrate organs. Nat Ecol Evol 1, 0072 (2017). https://doi.org/10.1038/s41559-017-0072
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