Abstract
Viviparity has evolved from oviparity approximately 142 times among vertebrates. Different theories have been proposed to explain the evolution of each of its traits in the different taxa. None, however, is applicable to all the viviparous vertebrates, since the derived ecological advantages such as controlling incubating temperature or protecting eggs against predation differ amongst clades. Most theories have been developed under a co-adaptive perspective, whereas less attention has been paid to conflict. We developed a broad panorama of the gradual evolution, from oviparity to advanced forms of viviparity, that includes the different environmental and co-adaptive selective pressures that have been suggested to be at the root of the different instances of viviparity and of the diverse maternal–foetal adaptations for nutrient transfer seen amongst vertebrates. Furthermore, we highlight the importance of conflict as a crucial driver of the evolution of many of those traits, including the evolution of epigenetic control of maternal resources. We suggest that the different types of matrotrophic viviparity, and probably also some reversals to oviparity, have been the result of an antagonistic coevolution between mothers, fathers and offspring, and their genomes. We additionally suggest that the appearance of a trait that allowed or favoured the evolution of internal development and matrotrophy generates a new selective environment that promotes further adaptations or counteradaptations, leading to the observed diversity of forms of embryonic development, nourishment, and transfer of maternal nutrients, and ultimately to the diversity of extant viviparous taxa.
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References
Adams SM, Biazik JM, Thompson MB, Murphy CR (2005) Cyto-epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: a new placental morphotype. J Morphol 264:264–276
Albergotti LC, Guillette LJ Jr (2011) Viviparity in reptiles: evolution and reproductive endocrinology. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates. Elsevier, Amsterdam, pp 247–275
Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL (2002) Influence of maternal size on placental, fetal and postnatal growth in the horse. I Development in Utero Reproduction 123:445–453
Amoroso EC (1960) Viviparity in fishes. Symp Zool S 1:153–181
Andrews RM (1997) Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention. J Zool 243:579–595
Andrews RM, Rose BR (1994) Evolution of viviparity: constraints on egg retention. Physiol Zool 67:1006–1024
Andrews SC, Wood MD, Tunster SJ, Barton SC, Surani MA, John RM (2007) Cdkn1c (p57Kip2) is the major regulator of embryonic growth within its imprinted domain on mouse distal chromosome 7. BMC Dev Biol 7:53. https://doi.org/10.1186/1471-213X-7-53
Arnqvist G, Rowe L (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789. https://doi.org/10.1038/415787a
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton, NJ
Baker J, Liu J-P, Robertson EJ, Efstratiadis A (1993) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73–82. https://doi.org/10.1016/S0092-8674(05)80085-6
Balshine S (2012) Patterns of parental care in vertebrates. In: Royle J, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 62–80
Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N (1991) The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349:84–87. https://doi.org/10.1038/349084a0
Beck CW (1998) Mode of fertilization and parental care in anurans. Dev Biol 55:439–449
Benun Sutton F, Wilson AB (2019) Where are all the moms? External fertilization predicts the rise of male parental care in bony fishes. Evolution 73(12):2451–2460
Bercu BB, Hyashi A, Poth M, Alexandrova M, Solof MS, Donahoe PK (1980) Luteinizing hormone-releasing hormone-induced delay of parturition. Endocrinology 107:504–508. https://doi.org/10.1210/endo-107-2-504
Blacher P, Huggins TJ, Bourke AFG (2017) Evolution of ageing, costs of reproduction and the fecundity – longevity trade-off in eusocial insects. Proc R Soc B 284:20170380. https://doi.org/10.1098/rspb.2017.0380
Blackburn DG (1992) Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Am Zool 32:313–321
Blackburn DG (1994) Standardized criteria for the recognition of embryonic nutritional patterns in squamate reptiles. Copeia 1994:925–935
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. https://doi.org/10.1002/(Sici)1097-010x(199811/12)282:4/5%3c560::Aid-Jez10%3e3.3.Co;2-A
Blackburn DG (1999) Viviparity and oviparity: Evolution and reproductive strategies. In: Knobil TE, Neill JD (eds) Encyclopedia of Reproduction. Academic Press, New York, pp 994–1003
Blackburn DG (2000) Classification of the reproductive patterns of amniotes. Herpetol Monogr 14:371–377
Blackburn DG (2015) Viviparous placentotrophy in reptiles and the parent-offspring conflict. J Exp Zool B 324:532–548. https://doi.org/10.1002/jez.b.22624
Blackburn DG (2015) Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis. J Morphol 276:961–990. https://doi.org/10.1002/jmor.20272
Blackburn DG, Flemming AF (2009) Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles. J Exp Zool B 312:579–589. https://doi.org/10.1002/jez.b.21234
Blackburn DG, Evans HE, Vitt LJ (1985) The evolution of fetal nutritional adaptations. Fortschr Zool 30:437–439
Bowman CE, Arany Z, Wolfgang MJ (2021) Regulation of maternal–fetal metabolic communication. Cell Mol Life Sci 78:1455–1486
Buckley D, Alcobendas M, García-París M, Wake MH (2007) Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. Evol Dev 9:105–115. https://doi.org/10.1111/j.1525-142X.2006.00141.x
Buckley D (2012) Evolution of viviparity in salamanders (Amphibia, Caudata). In: eLS , pp 1–13. https://doi.org/10.1002/9780470015902.a0022851
Buckling A, Rainey PB (2002) Antagonistic coevolution between a bacterium and a bacteriophage. Proc R Soc Lond B 269:931–936. https://doi.org/10.1098/rspb.2001.1945
Burley N (1981) Sex ratio manipulation and selection for attractiveness. Science 211:721–722
Burt A, Trivers R (1998) Genetic conflicts in genomic imprinting. Proc R Soc Lond B 265:2393–2397
Callard IP, Fileti LA, Perez LE, Sorbera LA, Giannoukos G, Klosterman LL, Tsang P, McCracken JA (1992) Role of the corpus luteum and progesterone in the evolution of vertebrate viviparity. Integr Comp Biol 32:264–275. https://doi.org/10.1093/icb/32.2.264
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–48
Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A (2003) Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. P Natl Acad Sci USA 100:8292–8297. https://doi.org/10.1073/pnas.1532175100
Chiba Y, He B, Yoshizaki K et al (2019) The transcription factor AmeloD stimulates epithelial cell motility essential for tooth morphology. J Biol Chem 294:3406–3418. https://doi.org/10.1074/jbc.RA118.005298
Chuong EB, Tong W, Hoekstra HE (2010) Maternal-fetal conflict: rapidly evolving proteins in the rodent placenta. Mol Biol Evol 27:1221–1225. https://doi.org/10.1093/molbev/msq034
Cohick WS, Clemmons DR (1993) The insulin-like growth factors. Annu Rev Physiol 55:131–153
Compagno LVJ (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date, vol. 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO species catalogue for fishery purposes no 1, vol. 2, Rom
Constância M, Hemberger M, Hughes J et al (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945–948. https://doi.org/10.1038/nature00819
Costa WJEM, Amorim PF, Mattos JLO (2016) Molecular phylogeny and evolution of internal fertilization in South American seasonal cynopoeciline killifishes. Mol Phylogenet Evol 95:94–99. https://doi.org/10.1016/j.ympev.2015.11.011
Crespi B, Semeniuk C (2004) Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am Nat 163:635–653. https://doi.org/10.1086/382734
Daneshfozouna H, Panjvinib F, Ghorbanic F, Farahmandd H (2015) A review of epigenetic imprints in aquatic animals. Fish Aquac J 6:1–3. https://doi.org/10.4172/2150-3508.1000119
Dawkins R, Carlise TR (1976) Parental investment, mate desertion and fallacy. Nature 262:131–133
DeChiara TM, Efstratiadis A, Robertson EJ (1990) A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345:78–80
DeChiara TM, Robertson EJ, Efstratiadis A (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–859. https://doi.org/10.1016/0092-8674(91)90513-X
Dopazo H, Alberch P (1994) Preliminary results on optional viviparity and intrauterine siblicide in Salamandra salamandra populations from Northern Spain. Mertensiella 4:125–137
Duvillié B, Cordonnier N, Deltour L, Dandoy-Dron F, Itier JM, Monthioux E, Jami J, Joshi RL, Bucchuni D (1997) Phenotypic alterations in insulin-deficient mutant mice. P Natl Acad Sci USA 94:5137–5140. https://doi.org/10.1073/pnas.94.10.5137
Duvillié B, Bucchini D, Tang T, Jami J, Pàldi A (1998) Imprinting at the mouse Ins2 locus: evidence for cis- and trans-allelic interactions. Genomics 47:52–57. https://doi.org/10.1006/geno.1997.5070
Einum S, Fleming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567. https://doi.org/10.1038/35014600
Faber JJ, Thornburg KL, Binder ND (1992) Physiology of placental transfer in mammals. Am Zool 32:343–354
Fowden AL, Sibley C, Reik W, Constancia M (2006) Imprinted genes, placental development and fetal growth. Horm Res 65:50–58. https://doi.org/10.1159/000091506
Frank D, Fortino W, Clark L, Musalo R, Wang W, Saxena A, Li C-M, Reik W, Ludwig T, Tycko B (2002) Placental overgrowth in mice lacking the imprinted gene Ipl. P Natl Acad Sci USA 99:7490–7495. https://doi.org/10.1073/pnas.122039999
Gabory A, Ripoche MA, Le Digarcher A et al (2009) H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development 136:3413–3421. https://doi.org/10.1242/dev.036061
Geist KS, Strassmann JE, Queller DC (2019) Family quarrels in seeds and rapid adaptive evolution in Arabidopsis. P Natl Acad Sci USA 116:9463–9468. https://doi.org/10.1073/pnas.1817733116
Ghalambor CK, Reznick DN, Walker JA (2004) Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am Nat 164:38–50. https://doi.org/10.1086/421412
Giddings SJ, King CD, Harman KW, Flood JF, Carnaghi LR (1994) Allele specific inactivation of insulin 1 and 2, in the mouse yolk sac, indicates imprinting. Nat Genet 6:310–313. https://doi.org/10.1038/ng0394-310
Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128. https://doi.org/10.1126/science.286.5437.126
Gilmore RG, Dodrill JW, Linley PA (1983) Reproduction and embryonic development of the sand tiger shark Odontaspis taurus (Refinesque). Fish Bull 81:201–226
Gilmore RG, Putz O, Dodrill JW (2005) Oophagy, intrauterine cannibalism and reproductive strategy in lamnoid sharks. In: Hamlett WC (ed) Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, batoids and chimaeras. Science Publishers, Enfield, NH, pp 435–462
Godfray HCT (1995) Signaling of need between parents and young: parent-offspring conflict and sibling rivalry. Am Nat 146:1–24
Greven H, Grossherr M (1992) Adelphophagy and oophagy in Ameca splendens Miller and Fitzsimons, 1971 (Goodeidae, Teleostei). Z Fischkd 12:193–197
Griffith OW, Wagner GP (2017) The placenta as a model for understanding the origin and evolution of vertebrate organs. Nat Ecol Evol 1:0072. https://doi.org/10.1038/s41559-017-0072
Griffith OW, Brandley MC, Belov K, Thompson MB (2016) Allelic expression of mammalian imprinted genes in a matrotrophic lizard, Pseudemoia entrecasteauxii. Dev Genes Evol 226:79–85. https://doi.org/10.1007/s00427-016-0531-x
Griffith OW, Brandley MC, Whittington CM, Belov K, Thompson MB (2017) Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes. Gen Comp Endocrinol 244:19–29. https://doi.org/10.1016/j.ygcen.2016.04.017
Gross MT, Sargent RC (1985) The evolution of male and female parental care in fishes. Am Zool 25:807–822
Guex GD, Chen PS (1986) Epitheliophagy: Intrauterine cell nourishment in the viviparous alpine salamander, Salamandra atra (Laur.). Experientia 42:1205–1218. https://doi.org/10.1007/BF01946392
Guillette LJ, Jones RE (1982) Further observations on arginine vasotocin-induced oviposition and parturition in lizards. J Herpetol 16:140–144
Guillette J, Louis J, DeMarco V, Palmer BD (1991) Exogenous progesterone or indomethacin delays parturition in the viviparous lizard Sceloporus jarrovi. Gen Comp Endocrinol 81:105–112
Guillette LJ, Propper CR, Cree A, Doresl RM (1991) Endocrinology of oviposition in the tuatara (Sphenodon punctatus)—II. Plasma arginine vasotocin concentrations during natural nesting. Comp Biochem Physiol A 100:819–822. https://doi.org/10.1016/0300-9629(91)90298-Q
Hagmayer A, Furness AI, Reznick DN, Dekker ML, Pollux BJA (2020) Predation risk shapes the degree of placentation in natural populations of live-bearing fish. Ecol Lett 23:831–840. https://doi.org/10.1111/ele.13487
Haig D (1993) Genetic conflicts in human pregnancy. Q Rev Biol 68:495–532
Haig D (1996) Placental hormones, genomic imprinting, and maternal-fetal communication. J Evol Biol 9:357–380. https://doi.org/10.1046/j.1420-9101.1996.9030357.x
Haig D (2000) The kinship theory of genomic imprinting. Annu Rev Ecol Syst 31:9–32
Haig D (2004) Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet 38:553–585. https://doi.org/10.1146/annurev.genet.37.110801.142741
Haig D, Westoby M (1989) Parent-specific gene expression and the triploid endosperm. Am Nat 134:147–155. https://doi.org/10.1086/284971
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. Phil Trans R Soc B 333:1–13. https://doi.org/10.1098/rstb.1991.0057
Hamlett WC (1999) Placenta and placental analogues in elasmobranchs. In: Knobil TE, Neill JD (eds) Encyclopedia of Reproduction. Academic Press, New York, pp 197–206
Hamlett WC, Hysell MK (1998) Uterine specializations in elasmobranchs. J Exp Zool 282:438–459
Hamlett WC, Kormanik G, Storrie M, Stevens B, Walker TI (2005) Chondrichthyan parity, lecithotrophy and matrotrophy. In: Hamlett WC (ed) Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras. Science Publishers, Enfield, NH, pp 395–434
Harrison A (2013) Size-assortative pairing and social monogamy in a neotropical lizard, Anolis limifrons (Squamata: Polychrotidae). Breviora 534:1–9. https://doi.org/10.3099/534.1
Hayakawa Y, Munehara H (2001) Facultatively internal fertilization and anomalous embryonic development of a non-copulatory sculpin Hemilepidotus gilberti Jordan and Starks (Scorpaeniformes: Cottidae). J Exp Mar Biol Ecol 256:51–58. https://doi.org/10.1016/S0022-0981(00)00303-8
Hayakawa Y, Munehara H (2003) Comparison of ovarian functions for keeping embryos by measurement of dissolved oxygen concentrations in ovaries of copulatory and non-copulatory oviparous fishes and viviparous fishes. J Exp Mar Biol Ecol 295:245–255. https://doi.org/10.1016/S0022-0981(03)00297-1
Helmstetter AJ, Papadopulos AST, Igea J, Van Dooren TJM, Leroi AM, Savolainen V (2016) Viviparity stimulates diversification in an order of fish. Nat Commun 7:11271. https://doi.org/10.1038/ncomms11271
Hollenberg F, Wourms JP (1994) Ultrastructure and protein uptake of the embryonic trophotaeniae of four species of goodeid fishes (Teleostei: Atheriniformes). J Morphol 219:105–129
Hollenberg F, Wourms JP (1995) Embryonic growth and maternal nutrient sources in goodeid fishes (Teleostei: Cyprinodontiformes). J Exp Zool A 271:379–394
Kahn AT, Schwanz LE, Kokko H (2013) Paternity protection can provide a kick-start for the evolution of male-only parental care. Evolution 67:2207–2217. https://doi.org/10.1111/evo.12103
Kalscheuer VM, Mariman EC, Schepens MT, Rehder H, Ropers H-H (1993) The insulin-like growth factor type-2 receptor gene is imprinted in the mouse but not in humans. Nat Genet 5:74–78
Kaneko-Ishino T, Kohda T, Ishino F (2003) The regulation and biological significance of genomic imprinting in mammals. J Biochem 133:699–711. https://doi.org/10.1093/jb/mvg090
Kaye MD, Jones WR, Anderson DT (1972) Immunology and placentation in viviparous invertebrates. J Reprod Fertil 1972:335–336. https://doi.org/10.1530/jrf.0.0310335
Kent GC (2018) Animal reproductive system. Encyclopedia Britannica, https://www.britannica.com/science/animal-reproductive-system
Klisch K, Mess A (2007) Evolutionary differentiation of cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta 28:353–360. https://doi.org/10.1016/j.placenta.2006.03.014
Kornfeld S, Mellman I (1989) The biogenesis of lysosomes. Annu Rev Cell Dev Biol 5:483–525
Kunz Y (2004) Developmental biology of teleost fishes. Springer, Dordrecht
Kupfer A, Kramer A, Himstedt W, Greven H (2006) Copulation and egg retention in an oviparous Caecilian (Amphibia: Gymnophiona). Zool Anz 244:223–228. https://doi.org/10.1016/j.jcz.2005.12.001
Kupfer A, Müller H, Antoniazzi MM, Jared C, Greven H, Nussbaum RA, Wilkinson M (2006) Parental investment by skin feeding in a caecilian amphibian. Nature 440:926–929. https://doi.org/10.1038/nature04403
Kupfer A, Maxwell E, Reinhard S, Kuehnel S (2016) The evolution of parental investment in caecilian amphibians: a comparative approach. Biol J Linn Soc 119:4–14. https://doi.org/10.1111/bij.12805
Lau MMH, Stewart CEH, Liu Z et al (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8:2953–2963. https://doi.org/10.1101/gad.8.24.2953
Lefebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA (1998) Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet 20:163–169. https://doi.org/10.1038/2464
Li Y, Behringer RR (1998) Esx1 is an X-chromosome-imprinted regulator of placental development and fetal growth. Nat Genet 20:309–311. https://doi.org/10.1038/3129
Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science (new York NY) 284:330–333. https://doi.org/10.1126/science.284.5412.330
Lombardi J, Wourms JP (1979) Structure, function, and evolution of trophotaeniae, placental analogues of viviparous fishes. Am Zool 19:976
Long JA, Mark-Kurik E, Johanson Z et al (2014) Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517:196–199. https://doi.org/10.1038/nature13825
Ludwig T, Eggenschwiler J, Fisher P, D’Ercole AJ, Davenport ML, Efstratiadis A (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in igf2 and igf1r null backgrounds. Dev Biol 535:517–535
Macías Garcia C, Ramirez E (2005) Evidence that sensory traps can evolve into honest signals. Nature 434:501–505. https://doi.org/10.1038/nature03351.1
MacKay AB, Mhanni AA, McGowan RA, Krone PH (2007) Immunological detection of changes in genomic DNA methylation during early zebrafish development. Genome 50:778–785. https://doi.org/10.1139/G07-055
Magurran AE, Seghers BH (1994) A cost of sexual harassment in the guppy, Poecilia reticulata. Proc R Soc Lond B 258:89–92
Mank JE, Promislow DEL, Avise JC (2005) Phylogenetic perspectives in the evolution of parental care in ray-finned fishes. Evolution 59:1570–1578. https://doi.org/10.1554/04-734.1.s1
Marsh-Matthews E, Deaton R (2006) Resources and offspring provisioning: A test of the Trexler-DeAngelis model for matrotrophy evolution. Ecology 87:3014–3020. https://doi.org/10.1890/0012-9658(2006)87[3014:RAOPAT]2.0.CO;2
Matoba S, Nakamuta S, Miura K, Hirose M, Shiura H, Kohda T, Nakamuta N, Ohuda A (2019) Paternal knockout of Slc38a4/SNAT4 causes placental hypoplasia associated with intrauterine growth restriction in mice. P Natl Acad Sci USA 116:21047–21053. https://doi.org/10.1073/pnas.1907884116
Matsushima N, Kawata M (2005) The choice of oviposition site and the effects of density and oviposition timing on survivorship in Rana japonica. Ecol Res 20:81–86. https://doi.org/10.1007/s11284-004-0010-0
McNamara JM, Houston AI, Barta Z, Osorno JL (2003) Should young ever be better off with one parent than with two? Behav Ecol 14:301–310. https://doi.org/10.1093/beheco/14.3.301
Meek SE (1904) The fresh-water fishes of Mexico north of the Isthmus of Tehuantepec. Field Columbian Mus Publ 93. Zool Ser 5:i–lxiii:1–252
Meisner AD, Burns JR (1997) Viviparity in the halfbeak genera Dermogenys and Nomorhamphus (Teleostei: Hemiramphidae). J Morphol 234:295–317. https://doi.org/10.1002/(SICI)1097-4687(199712)234:3%3c295::AID-JMOR7%3e3.0.CO;2-8
Mess A, Carter AM (2007) Evolution of the placenta during the early radiation of placental mammals. Comp Biochem Physiol A 148:769–779. https://doi.org/10.1016/j.cbpa.2007.01.029
Miller RR, Fitzsimons JM (1971) Ameca splendens, a new genus and species of goodeid fish from western Mexico, with remarks on the classification of the Goodeidae. Copeia 8:1–3
Montserrat M, Bas C, Magalhães S, Sabelis MW, De Roos AM, Janssen A (2007) Predators induce egg retention in prey. Oecologia 150:699–705. https://doi.org/10.1007/s00442-006-0527-8
Moore T (2012) Review: Parent-offspring conflict and the control of placental function. Placenta 33:S33–S36. https://doi.org/10.1016/j.placenta.2011.11.016
Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7:45–49. https://doi.org/10.1016/0168-9525(91)90230-N
Morrison KR, Ngo V, Cardullo RA, Reznick DN (2017) How fish eggs are preadapted for the evolution of matrotrophy. Proc R Soc B 284:20171342. https://doi.org/10.1098/rspb.2017.1342
Mossman HW (1991) Comparative morphogenesis of the fetal membranes accesso and uterine structures. Placenta 12:1–5
Motz VA, Callard IP (1988) Seasonal variations in oviductal activity, extensibility, and tensile strength in Chrysemys picta. Gen Comp Endocrinol 72:453–460. https://doi.org/10.1016/0016-6480(88)90168-2
Murphy BF, Thompson MB (2011) 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. https://doi.org/10.1007/s00360-011-0584-0
Murphy WJ, Thomerson JE, Collier GE (1999) Phylogeny of the Neotropical killifish family Rivulidae (Cyprinodontiformes, Aplocheiloidei) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 13:289–301. https://doi.org/10.1006/mpev.1999.0656
O’Neill MJ, Ingram RS, Vrana PB, Tilghman SM (2000) Allelic expression of IGF2 in marsupials and birds. Dev Genes Evol 210:18–20. https://doi.org/10.1007/PL00008182
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. P Natl Acad Sci USA 104:12404–12409. https://doi.org/10.1073/pnas.0705048104
Okamura K, Hagiwara-Takeuchi Y, Li T, Vu TH, Hirai M, Hattori M, Sakaki Y, Hoffman AR, Ito T (2000) Comparative genome analysis of the mouse imprinted gene impact and its nonimprinted human homolog IMPACT: toward the structural basis for species-specific imprinting. Genome Res 10:1878–1889. https://doi.org/10.1101/gr.139200
Osorno JL, Székely T (2004) Sexual conflict and parental care in magnificent frigatebirds: Full compensation by deserted females. Dev Biol 68:337–342. https://doi.org/10.1016/j.anbehav.2003.06.027
Ostrovsky AN, Lidgard S, Gordon DP, Schwaha T, Genikhovich G, Ereskovsky AV (2016) Matrotrophy and placentation in invertebrates: a new paradigm. Biol Rev 91:673–711. https://doi.org/10.1111/brv.12189
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567. https://doi.org/10.1111/j.1469-185X.1970.tb01176.x
Parker GA (1974) Courtship persistence and female-guarding as male time investment strategies. Behaviour 48:157–184
Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm Competition and the Evolution of Animal Mating Systems. Academic Press, London, pp 1–60
Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Phil Trans R Soc B 361:235–259. https://doi.org/10.1098/rstb.2005.1785
Pearsall RS, Shibata H, Brozowska A, Yoshino K, Okuda K, DeJong PJ, Plass C, Chapman VM, Hayashizaki Y, Held WA (1996) Absence of imprinting in U2AFBPL, a human homologue of the imprinted mouse gene U2afbp-rs. Biochem Biophys Res Commun 222:171–7. S0006–291X(96)90716–0 [pii] https://doi.org/10.1006/bbrc.1996.0716
Pickford GE (1952) Induction of a spawning reflex in hypophysectomized killifish. Nature 170:807–808
Pollux BJA, Reznick DN (2011) Matrotrophy limits a female’s ability to adaptively adjust offspring size and fecundity in fluctuating environments. Funct Ecol 25:747–756. https://doi.org/10.1111/j.1365-2435.2011.01831.x
Pollux BJA, Pires MN, Banet AI, Reznick DN (2009) Evolution of placentas in the fish family Poeciliidae: an empirical study of macroevolution. Annu Rev Ecol Evol S 40:271–289. https://doi.org/10.1146/annurev.ecolsys.110308.120209
Recknagel H, Kamenos NA, Elmer KR (2021) Evolutionary origins of viviparity consistent with palaeoclimate and lineage diversification. J Evol Biol 34:1167–1176. https://doi.org/10.1111/jeb.13886
Reik W, Constância M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, Tycko B, Sibley C (2003) Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 547:35–44. https://doi.org/10.1113/jphysiol.2002.033274
Renfree MB, Suzuki S, Kaneko-Ishino T (2013) The origin and evolution of genomic imprinting and viviparity in mammals. Phil Trans R Soc B 368:20120151. https://doi.org/10.1098/rstb.2012.0151
Reznick DN, Mateos M, Springer MS (2002) independent origins and rapid fish genus Poeciliopsis. Science 298:1018–1020. https://doi.org/10.1126/science.1076018
Reznick DN, Meredith R, Collette BB (2007) Independent evolution of complex life history adaptations in two families of fishes, live-bearing halfbeaks (Zenarchopteridae, Beloniformes) and Poeciliidae (Cyprinodontiformes). Evolution 61:2570–2583. https://doi.org/10.1111/j.1558-5646.2007.00207.x
Riesch R, Plath M, Schlupp I, Tobler M, Brian Langerhans R (2014) Colonisation of toxic environments drives predictable life-history evolution in livebearing fishes (Poeciliidae). Ecol Lett 17:65–71. https://doi.org/10.1111/ele.12209
Roberts RM, Green JA, Schulz LC (2016) The evolution of the placenta. Reproduction 152:R179–R189. https://doi.org/10.1530/REP-16-0325
Rodao M, Montagne J, Clivio GA, Papa NG, Larrosa GC (2015) Sperm and egg envelope ultrastructure and some considerations on its evolutionary meaning. In: Berois N, García G, de Sá RO (eds) Annual Fishes: Life History Strategy, Diversity, and Evolution. CRC Press, Boca Raton, pp 47–62
Royle NJ, Smiseth PT, Kölliker M (eds) (2012) The evolution of parental care. Oxford University Press, Oxford
Saldivar Lemus Y, Vielle-Calzada J-P, Ritchie MG, Macías García C (2017) Asymmetric paternal effect on offspring size linked to parent-of-origin expression of an insulin-like growth factor. Ecol Evol 7:4465–4474. https://doi.org/10.1002/ece3.3025
San Mauro D, Gower DJ, Müller H, Loader SP, Zardoya R, Nussbaum RA, Wilkinson M (2014) Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Mol Phylogenet Evol 73:177–189. https://doi.org/10.1016/j.ympev.2014.01.009
Savage J (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, Chicago
Schneider JM (1999) Delayed oviposition: a female strategy to counter infanticide by males? Behav Ecol 10:567–571
Schrader M, Travis J (2008) Testing the viviparity-driven-conflict hypothesis: parent-offspring conflict and the evolution of reproductive isolation in a poeciliid fish. Am Nat 172:806–817. https://doi.org/10.1086/592999
Schwartz TS, Bronikowski AM (2016) Evolution and function of the insulin and insulin-like signaling network in ectothermic reptiles: some answers and more questions. Integr Comp Biol 56:171–184
Shibukawa K, Tran DD, Tran LX (2012) Phallostethus cuulong, a new species of priapiumfish (Actinopterygii: Atheriniformes: Phallostethidae) from the Vietnamese Mekong. Zootaxa 51:45–51
Shine R (2014) Evolution of an evolutionary hypothesis: a history of changing ideas about the adaptive significance of viviparity in reptiles. J Herpetol 48:147–161. https://doi.org/10.1670/13-075
Sibly RM, Kodric-Brown A, Luna SM, Brown JH (2018) The shark-tuna dichotomy: Why tuna lay tiny eggs but sharks produce large offspring. R Soc Open Sci 5:180453. https://doi.org/10.1098/rsos.180453
Smith KK (2015) Placental evolution in therian mammals. In: Dial KP, Shubin N, Brainerd EL (eds) Great transformations in vertebrate evolution. University of Chicago Press, Chicago, pp 205–225
Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Stud Behav 22:1–63. https://doi.org/10.1016/S0065-3454(08)60404-0
Springer S (1948) Oviphagous embryos of the sand shark, Carcharias taurus. Copeia 1948:153–157. https://doi.org/10.2307/1438449
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stewart JR (1992) Placental structure and nutritional provision to embryos in predominantly lecithotrophic viviparous reptiles. Integr Comp Biol 32:303–312. https://doi.org/10.1093/icb/32.2.303
Stewart JR, Blackburn DG (1988) Reptilian placentation: structural diversity and terminology. Copeia 1988:839–852
Stewart JR, Blackburn DG (2014) Viviparity and placentation in lizards. In: Rheubert JL, Siegel DS, Trauth SE (eds) Reproductive biology and phylogeny of lizards and tuatara. CRC Press, Boca Raton, FL, pp 448–563
Stewart JR, Thompson MB (1996) Evolution of reptilian placentation: development of extraembryonic membranes of the Australian scincid lizards, Bassiana duperreyi (oviparous) and Pseudemoia entrecasteauxii (viviparous). J Morphol 227:349–370. https://doi.org/10.1002/(sici)1097-4687(199603)227:3%3c349::aid-jmor6%3e3.0.co;2-0
Stewart JR, Thompson MB (2000) Evolution of placentation among squamate reptiles: recent research and future directions. Comp Biochem Physiol A 127:411–431. https://doi.org/10.1016/S1095-6433(00)00273-7
Stockley P, Gage MJT, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954
Tan HH, Lim KKP (2013) Three new species of freshwater halfbeaks (Teleostei: Zenarchopteridae: Hemirahamphodon) from Borneo. Raffles Bull Zool 61:735–747
Tarwater CE, Arcese P (2017) Young females pay higher costs of reproduction in a short-lived bird. Behav Ecol Sociobiol 71:84. https://doi.org/10.1007/s00265-017-2309-1
Thiem L (2020) Hold on for one more day: oviductal egg retention as a mechanism for flexible reproductive phenology in eastern musk turtles (Sternotherus odoratus). MSc thesis, Austin Peay State University
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. https://doi.org/10.1007/s00360-005-0048-5
Thompson MB, Adams SM, Herbert JF, Biazik JM, Murphy CR (2004) Placental function in lizards. Int Congr Ser 1275:218–225. https://doi.org/10.1016/j.ics.2004.08.055
Tilghman SM (1999) The sins of the fathers and mothers: Genomic imprinting in mammalian development. Cell 96:185–193. https://doi.org/10.1016/S0092-8674(00)80559-0
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Selection and the Descent of Man 1871–1971. Aldine de Gruyter, New York, pp 134–179
Trivers RL (1974) Parent-Offspring Conflict Am Zool 14:249–264. https://doi.org/10.1093/icb/14.1.249
Trivers RL (1985) Social evolution. Cummings Publishing Co., Menlo Park, CA
Turner CL (1936) The absorptive processes in the embryos of Parabrotula dentiens, a viviparous, deep-sea Brotulid fish. J Morphol 59:313–325. https://doi.org/10.1002/jmor.1050590205
Turner CL (1940) Pseudoamnion, pseudochorion, and follicular pseudoplacenta in poeciliid fishes. J Morphol 67:59–89
Tycko B, Morison IM (2002) Physiological functions of imprinted genes. J Cell Physiol 192:245–258. https://doi.org/10.1002/jcp.10129
Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580. https://doi.org/10.1111/j.1365-294X.2008.03772.x
Uribe MC, García Alarcón A (2005) The ovary of viviparous teleosts. Morphological differences between the ovaries of Goodea atripinnis and Ilydon whitei (Goodeidae). In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publication, Homestead, FL, pp 217–235
Wake MH (1977) The reproductive biology of caecilians: an evolutionary perspective. In: Taylor DH, Guttman SI (eds) The reproductive biology of amphibians. Plenum, New York, pp 73–101
Wake MH (1977) Fetal maintenance and its evolutionary significance in the Amphibia: Gymnophiona. J Herpetol 11:379–386
Wake MH (1980) The reproductive biology of Nectophrynoides malcolmi (Amphibia: Bufonidae), with comments on the evolution of reproductive modes in the genus Nectophrynoides. Copeia 1980:193–209
Wake MH (1992) Evolutionary scenarios, homology and convergence of structural specializations for vertebrate viviparity. Integr Comp Biol 32:256–263. https://doi.org/10.1093/icb/32.2.256
Wake MH (2015) Fetal adaptations for viviparity in amphibians. J Morphol 276:941–960. https://doi.org/10.1002/jmor.20271
Wake MH, Hanken J (1982) Development of the skull of Dermophis mexicanus (amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173:203–223. https://doi.org/10.1002/jmor.1051730208
Wang S, Yuen SSF, Randall DJ, Hung CY, Tsui TKN, Poon WL, Lai JCC, Zhang Y, Lin H (2008) Hypoxia inhibits fish spawning via LH-dependent final oocyte maturation. Comp Biochem Physiol C 148:363–369. https://doi.org/10.1016/j.cbpc.2008.03.014
Whittington CM, van Dyke JU, Liang SQT, Edwards SV, Shine R, Thompson MB, Grueber CE (2022) Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy. Biol Rev (published online, https://doi.org/10.1111/brv.12836)
Wiklund C, Fagerström T (1977) Why do males emerge before females? Oecologia 31:153–158. https://doi.org/10.1007/BF00346917
Wildman DE, Chen C, Grossman LI, Goodman M, Romero R (2006) Evolution of the mammalian placenta revealed by phylogenetic analysis. P Natl Acad Sci USA 103:3203–3208
Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4:359–368. https://doi.org/10.1038/nrg1062
Wooding P, Burton G (2008) Comparative placentation: structures, functions and evolution. Springer, Berlin
Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410
Wourms JP (1981) Viviparity: The maternal-fetal relationship in fishes. Integr Comp Biol 21:473–515. https://doi.org/10.1093/icb/21.2.473
Wourms JP, Lombardi J (1992) Reflections on the evolution of piscine viviparity. Integr Comp Biol 32:276–293. https://doi.org/10.1093/icb/32.2.276
Wourms JP, Grove B, Lombardi J (1988) The maternal-embryonic relationship in viviparous fishes. In: Hoar W, Randall D (eds) Fish Physiology, vol 11B. Academic Press, New York, pp 1–134
Xavier F (1973) Le cycle des voies génitales femelles de Nectophrynoides occidentalis Angel, Amphibien Anoure vivipare. Z Zellforsch 140:509–534. https://doi.org/10.1007/BF00306677
Xie B, Zhang L, Zheng K, Luo C (2009) The evolutionary foundation of genomic imprinting in lower vertebrates. Chin Sci Bull 54:1354–1360. https://doi.org/10.1007/s11434-009-0149-8
Yokoe M, Takayama-Watanabe E, Saito Y, Kutsuzawa M, Fujita K, Ochi H, Nakauchi Y, Watanabe A (2016) A novel cysteine knot protein for enhancing sperm motility that might facilitate the evolution of internal fertilization in amphibians. PLoS ONE 11:e0160445. https://doi.org/10.1371/journal.pone.0160445
Yu S, Yu D, Lee E, Eckhaus M, Lee R, Corria Z, Accili D, Westphal H, Weisntein LS (1998) Variable and tissue-specific hormone resistance in heterotrimeric Gs protein α-subunit (Gsα) knockout mice is due to tissue-specific imprinting of the Gsα gene. Genetics 95:8715–8720. https://doi.org/10.1073/pnas.95.15.8715
Yu S, Gavrilova O, Chen H, Lee R, Liu J, Pacak K, Parlow AF, Quon M, Reitman ML, Weinstein LS (2000) Paternal versus maternal transmission of a stimulatory G-protein α subunit knockout produces opposite effects on energy metabolism. J Clin Invest 105:615–623. https://doi.org/10.1172/JCI8437
Yu S, Castle A, Chen M, Lee R, Takeda K, Weinstein LS (2001) Increased insulin sensitivity in Gsα knockout mice. J Biol Chem 276:19994–19998. https://doi.org/10.1074/jbc.M010313200
Zeh DW, Zeh JA (2000) Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays 22:938–946. https://doi.org/10.1002/1521-1878(200010)22:10%3c938::AID-BIES9%3e3.0.CO;2-9
Zúñiga-Vega JJ, Fuentes-G JA, Ossip-Drahos AG, Martins EP (2016) Repeated evolution of viviparity in phrynosomatid lizards constrained interspecific diversification in some life-history traits. Biol Lett 12:20160653. https://doi.org/10.1098/rsbl.2016.0653
Zwoinska M, Lind MI, Maklakov AA (2014) Sexual conflict: Male control of female longevity. Curr Biol 24:R196–R198. https://doi.org/10.1016/j.cub.2014.01.044
Acknowledgements
We thank Michael G. Ritchie for providing the parenthetical notation of the phylogeny of goodeids and for his comments on an earlier version of the manuscript, and Marcela Méndez-Janovitz and Nadia Neri-Vera for their guide during the construction of phylogenetic trees. YSL is grateful to the Doctorado en Ciencias Biomédicas (UNAM) and to CONACyT for providing a PhD scholarship (No. 46568). This manuscript was much improved thanks to the comments of two referees.
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Authors contributed equally to this work. YS-L conceived the review, conducted the literature search, and generated a first draft that was subsequently reworked jointly by both YS-L and CMG.
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Saldívar-Lemus, Y., Macías Garcia, C. Conflict and the evolution of viviparity in vertebrates. Behav Ecol Sociobiol 76, 68 (2022). https://doi.org/10.1007/s00265-022-03171-z
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DOI: https://doi.org/10.1007/s00265-022-03171-z