From incipient to substantial: Evolution of placentotrophy in a phylum of aquatic colonial invertebrates

Evolution

Volumn 67, Issue 5, 2013, Pages 1368-1382

  Ostrovsky, Andrew N ^a,b  

^a UNIVERSITY OF VIENNA   (Austria)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Brooding; Bryozoa; Cheilostomata; Matrotrophy; Oogenesis

Indexed keywords

ANATOMY; AQUATIC COMMUNITY; CLADISTICS; EVOLUTIONARY BIOLOGY; INVERTEBRATE; POLYMORPHISM;

ANIMAL; ARTICLE; BRYOZOA; EMBRYO DEVELOPMENT; GENETICS; HISTOLOGY; MOLECULAR EVOLUTION; OOCYTE DEVELOPMENT; PRENATAL DEVELOPMENT; REPRODUCTION;

ANIMALS; BRYOZOA; EMBRYONIC DEVELOPMENT; EVOLUTION, MOLECULAR; OOGENESIS; REPRODUCTION;

BRYOZOA; CHEILOSTOMATIDA; INVERTEBRATA; VERTEBRATA;

EID: 84876860850     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12039     Document Type: Article

References (107)

1. Adiyodi, K. G., and R. G. Adiyodi, eds. 1989. Reproductive biology of invertebrates. Vol. 4, Part A, Fertilization, development, and parental care. IBH Publishing Co. Pvt. Ltd., New Delhi, Bombay, Calcutta, Oxford.
2. Adiyodi, K. G., and R. G. Adiyodi. 1990. Reproductive biology of invertebrates. Vol. 4, Part B, Fertilization, development, and parental care. John Wiley and Sons, Chichester, New York, Brisbane, Toronto, Singapore.
3. Anderson, D. T. 1973. Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford, New York.
4. Arias, A., and D. Reznick. 2000. Life history of Phalloceros caudimaculatus: a novel variation on the theme of lifebearing in the family Poeciliidae. Copeia 2000:792-798.
5. Bermingham, J., and T. L. Wilkinson. 2009. Embryo nutrition in parthenogenetic viviparous aphids. Phys. Entomol. 34:103-109.
6. Blackburn, D. G. 1992. Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Amer. Zool. 32:313-321.
7. Blackburn, D. G. 1993. Chorioallantoic placentation in squamate reptiles - structure, function, development and evolution. J. Exp. Zool. 266:414-430.
8. Blackburn, D. G. 1999a. Placenta and placental analogs in reptiles and amphibians. Pp. 840-847 in E. Knobil and J. D. Neill, eds. Encyclopedia of reproduction. Academic Press, New York.
9. Blackburn, D. G. 1999b. Viviparity and oviparity: evolution and reproductive strategies. Pp. 994-1003 in E. Knobil and J. D. Neill, eds. Encyclopedia of reproduction. Academic Press, New York.
10. Blackburn, D. G. 1999c. Are viviparity and egg-guarding evolutionarily labile in squamates? Herpetologica 55:556-572.
11. Blackburn, D. G. 2005a. Evolutionary origins of viviparity in fishes. Pp. 303-317 in H. Rier and M. C. Uribe, eds. Viviparity in fishes. New Life Publications, Homestead, FL.
12. Blackburn, D. G. 2005b. Amniote perspectives on the evolution of viviparity. Pp. 319-340 in H. Rier and M. C. Uribe, eds. Viviparity in fishes. New Life Publications, Homestead, FL.
13. Blackburn, D. G. 2006. Squamate reptiles as model organisms for the evolution of viviparity. Herpetol. Monogr. 20:131-146.
14. Blackburn, D. G., H. E. Evans, and L. J. Vitt. 1985. The evoltuion of fetal nutritional adaptations. Fortschr. Zool. 30:437-439.
15. Boardman, R. S., A. H. Cheetham, D. B. Blake, J. Utgaard, O. L. Karklins, P. L. Cook, P. A. Sandberg, G. Lutaud, and T. S. Wood. 1983. Bryozoa (Part G, revised). Pp. 1-625 in R. A. Robinson, ed. Treatise on invertebrate paleontology, Vol. 1, Geological Society of America, Boulder, Colorado; Univ. of Kansas, Lawrence.
16. Brawand, D., W. Wahli, and H. Kaessmann. 2008. Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biol. 6:507-517.
17. Byrne, M. 1991. Developmental diversity in the starfish genus Patiriella (Asteroidea: Asterinidae). Pp. 499-508 in T. Yanagisawa, I. Yasumasu, C. Oguro, N. Suzuki, and T. Motokawa eds. Biology of echinodermata. A. A. Balkema, Rotterdam, The Netherlands.
18. Byrne, M., and A. Cerra. 1996. Evolution of intragonadal development in the diminutive asterinid sea stars Patiriella vivipara and P. parvivipara with an overview of development in the Asterinidae. Biol. Bull. 191:17-26.
19. Byrne, M., A. Cerra, and J. T. Villinski. 1999. Oogenic strategies in the evolution of development in Patiriella (Echinodermata: Asteroidea). Int. J. Invert. Rep. Dev. 36:195-202.
20. Cable, J., and R. C. Tinsley. 1991. Intra-uterine larval development of the polystomatid monogeneans, Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 103:253-266.
21. Cancino, J. M., and R. N. Hughes. 1988. The zooidal polymorphism and astogeny of Celleporella hyalina (Bryozoa: Cheilostomata). J. Zool. (Lond.) 215:167-181.
22. Corrêa, D. D. 1948. A embryologia de Bugula flabellata (J. V. Thompson) Bryozoa Ectoprocta. Bol. Fac. Fil. Ci. Letr. Univ. São Paulo, Zool. 13:7-71.
23. Dulvy, N. K., and J. D. Reynolds. 1997. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proc. Roy. Soc. B 264:1309-1315.
24. Dyrynda, P. E. J. 1981. A preliminary study of patterns of polypide generation-degeneration in marine cheilostome Bryozoa. Pp. 73-81 in G. P. Larwood and C. Nielsen, eds. Recent and fossil Bryozoa. Olsen and Olsen, Fredensborg, Denmark.
25. Dyrynda, P. E. J., and P. E. King. 1982. Sexual reproduction in Epistomia bursaria (Bryozoa: Cheilostomata), an endozooidal brooder without polypide recycling. J. Zool. (Lond.). 198:337-352.
26. Dyrynda, P. E. J., and P. E. King. 1983. Gametogenesis in placental and non-placental ovicellate cheilostome Bryozoa. J. Zool. (Lond.). 200:471-492.
27. Dyrynda, P. E. J., and J. S. Ryland. 1982. Reproductive strategies and life histories in the cheilostome marine bryozoans Chartella papyracea and Bugula flabellata. Mar. Biol. 71:241-256.
28. Eggleston, D. 1972. Patterns of reproduction in the marine Ectoprocta of the Isle of Man. J. Nat. Hist. 6:31-38.
29. Farley, R. D. 1996. Formation of maternal trophic structures for embryos of Paruroctonus mesaeensis (Scorpionida: Vejovidae). Rev. Suiss. Zool. HS 1:189-202.
30. Farley, R. D. 2001. Structure, reproduction and development. Pp. 13-77 in P. Brownell and G. Polis, eds. Scorpion biology and research. Oxford Univ. Press, Oxford, New York.
31. Flemming, A. F., and D. G. Blackburn. 2003. Evolution of placental specializations in viviparous African and South American lizards. J. Exp. Zool. 299A:33-47.
32. Francke, O. F. 1982. Parturition in scorpions (Arachnida, Scorpiones). Rev. Arachnol. 4:27-37.
33. Fuchs, J., M. Obst, and P. Sundberg. 2009. The first comprehensive molecular phylogeny of Bryozoa (Ectoprocta) based on combined analyses of nuclear and mitochondrial genes. Mol. Phylogenet. Evol. 52:225-233.
34. Galaktionov, K., and A. Dobrovolskij. 2003 The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Kluwer Academic Publishers, Boston, London, Dordrecht.
35. Giese, A. C., and J. S. Pearse, eds. 1974. Reproduction of marine invertebrates. Vol. 1, Acoelomate and pseudocoelomate metazoans. Academic Press, New York.
36. Giese, A. C., and J. S. Pearse, eds. 1975a. Reproduction of marine invertebrates Vol. 2, Entoprocts and lesser coelomates. Academic Press, New York.
37. Giese, A. C., and J. S. Pearse, eds. 1975b. Reproduction of marine invertebrates Vol. 3, Annelids and echiurans. Academic Press. New York.
38. Giese, A. C., and J. S. Pearse, eds. 1977. Reproduction of marine invertebrates. Vol. 4, Molluscs: gastropods and cephalopods. Academic Press. New York.
39. Giese, A. C., J. S. Pearse, and V. B. Pearse, eds. 1979. Reproduction of marine invertebrates. Vol. 5, Molluscs: pelecypods and lesser classes. Academic Press, New York.
40. Giese, A. C., J. S. Pearse, and V. B. Pearse, eds. 1991. Reproduction of marine invertebrates. Vol. 6, Echinoderms and lophophorates. Boxwood Press, Pacific Grove, CA.
41. Godeaux, J. E. A. 1990. Urochordata - Thaliacea. Pp. 453-469 in K. G. Adiyodi and R. G. Adiyodi, eds. Reproductive biology of invertebrates. Vol. 4, Part B: fertilization, development, and parental care. IBH Publishing Co. Pvt. Ltd., New Delhi, Bombay, Calcutta, Oxford.
42. Goodwin, N. B., N. K. Dulvy, and J. D. Reynolds. 2002. Life-history correlates of the evolution of life-bearing of fishes. Proc. Roy. Soc. B 357:259-267.
43. Gordon, D. P. 1977. The aging process in bryozoans. Pp. 335-376 in R. M. Woollacott and R. L. Zimmer, eds. Biology of bryozoans. Academic Press, New York, San Francisco, London.
44. Gordon, D. P. 2000. Towards a phylogeny of cheilostomes - morphological models of frontal wall/shield evolution. Pp. 17-37 in A. Herrera Cubilla and J. B. C. Jackson, eds. Proceedings of the 11th International Bryozoology Association Conference. Smithsonian Tropical Research Institute, Republic of Panama.
45. Gordon, D. P., and E. Voigt. 1996. The kenozooidal origin of the ascophorine hypostegal coelom and associated frontal shield. Pp. 89-107 in D. P. Gordon, A. M. Smith and J. A. Grant-Mackie, eds. Bryozoans in space and time. National Institute of Water and Atmospheric Research, Wellington.
46. Hagan, H. R. 1951. Embryology of viviparous insects. Ronald Press, New York.
47. Harmer, S. F. 1926. The Polyzoa of the Siboga Expedition. II. Cheilostomata Anasca. Rep. Siboga Exped. 28b:181-501. E. J. Brill, Leiden.
48. Heard, S. B., and D. L. Hauser, 1995. Key evolutionary innovations and their ecological mechanisms. Hist. Biol. 10:151-173.
49. Hoese, B., and H. H. Janssen. 1989. Morphological and physiological studies on the marsupium in terrestrial isopods. Monit. Zool. Ital., NS, 4:153-173.
50. Hughes, D. J. 1987. Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina. J. Zool. (Lond.). 212:691-711.
51. Knight, S., D. P. Gordon, and S. D. Lavery. 2011. A multi-locus analysis of phylogenetic relationships within cheilostome bryozoans supports multiple origins of ascophoran frontal shields. Mol. Phylogenet. Evol. 61:351-362.
52. Korneva, J. V. 2005. Placental type interactions and evolutionary trends of development of uterus in cestodes. J. Evol. Biochem. Phys. 41:552-560.
53. Lee, M. S. Y., and R. Shine. 1998. Reptilian viviparity and Dollo's law. Evolution 52:1441-1450.
54. Levin, L. F., and T. S. Bridges. 1995. Pattern and diversity in reproduction and development. Pp. 1-48 in L. McEdwards, ed. Ecology of marine invertebrate larvae. CRC Press, Boca Raton, London, New York, Washington, DC.
55. Lidgard, S., M. C. Carter, M. H. Dick, D. P. Gordon, and A. N. Ostrovsky. 2012. Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evol. Ecol. 26:233-257.
56. Lombardi, J. 1998. Comparative vertebrate reproduction. Kluwer Academic Publishers, Boston, Dordrecht, London.
57. Mank, J. E., D. E. L. Promislow, and J. C. Avise. 2005. Phylogenetic perspectives in the evolution of parental care in ray-finned fishes. Evolution 59:1570-1578.
58. Marcus, E. 1941. Sobre o desenvolvimento do bryozoario Synnotum aegyptiacum. Arq. Cirurg. Cl. Exp. 5:227-234.
59. Marsh-Matthews, E. 2011. Matrotrophy. Pp. 18-27 in J. Evans, A. Pilastro and I. Schlupp, eds. Ecology and evolution of poeciliid fishes. Univ. of Chicago Press, Chicago, IL.
60. Marsh-Matthews, E., R. Deaton, and M. Brooks. 2010. Survey of matrotrophy in lecithotrophic poeciliids. Pp. 255-258 in Uribe, M. C., and H. J. Grier, eds. Viviparous fishes II. New Life Publications, Homestead, Florida.
61. Meier, R., M. Kotrba, and P. Ferrar. 1999 Ovoviviparity and viviparity in the Diptera. Biol. Rev. 74:199-258.
62. Meredith, R. W., M. N. Pires, D. N. Resnick, and M. S. Springer. 2011. Molecular phylogenetic relationships and the coevolution of placentotrophy and superfetation in Poecilia (Poeciliidae: Cyprinodontiformes). Mol. Phylogenet. Evol. 59:148-157.
63. Moosburgger, M., T. Schwaha, M.G. Walzl, M. Obst, and A.N. Ostrovsky. 2012. The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata). Front. Zool. 9: 29. doi: 10.1186/174220139994-9201329.
64. Mossman, H.W. 1937. Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Inst. Washington, Contr. Embryol. 26:129-246.
65. Mukai, H., Y. Saito, and H. Watanabe. 1987. Viviparous development in Botrylloides (compound ascidians). J. Morph. 193:263-276.
66. Müller, G. B., and G. P. Wagner. 1991. Novelty in evolution: restructuring the concept. Ann. Rev. Ecol. Syst. 22:229-256.
67. Nielsen, C. 1981. On morphology and reproduction of Hippodiplosia insculpta and Fenestrulina malusii (Bryozoa, Cheilostomata). Ophelia 20:91-125.
68. Nielsen, C. 1990. Bryozoa Entoprocta. Pp. 201-209 in K. G. Adiyodi and R. G. Adiyodi, eds. Reproductive biology of invertebrates. Vol. 4, Part B: fertilization, development, and parental care. John Wiley and Sons, Chichester, New York, Brisbane, Toronto, Singapore.
69. Nitecki, M. H., ed. 1990. Evolutionary innovations. Univ. of Chicago Press, Chicago, IL.
70. Ostrovsky, A. N. 1998. Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida). Acta Zool. 79:287-318.
71. Ostrovsky, A. N. 2002. Brood chambers in cribrimorphs evolved by fusion of costae: further arguments. Pp. 247-255, in P. N. Wyse Jackson, C. J. Buttler and M. E. Spencer Jones, eds. Bryozoan studies 2001. A. A. Balkema Publishers, Lisse.
72. Ostrovsky, A. N. 2009. Evolution of the sexual reproduction in the bryozoan order Cheilostomata (Gymnolaemata). St Petersburg State University [In Russian with English summary].
73. Ostrovsky, A. N., M. H. Dick, and S. F. Mawatari. 2007. The internal-brooding apparatus in the bryozoan genus Cauloramphus (Cheilostomata: Calloporidae) and its inferred homology to ovicells. Zool. Sci. 25:36-52.
74. Ostrovsky, A. N., D. P. Gordon, and S. Lidgard. 2009a. Independent evolution of matrotrophy in the major classes of Bryozoa: transitions among reproductive patterns and their ecological background. Mar. Ecol. Prog. Ser. 378:113-124.
75. Ostrovsky, A. N., Grischenko, A. V., Taylor, P. D., Bock, and S. F. Mawatari. 2006. Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomical and evolutionary implications. J. Morph. 267:739-749.
76. Ostrovsky, A. N., A. O'Dea, and F. Rodrígues. 2009b. Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free-living cheilostomes. J. Morph. 270:1413-1430.
77. Ostrovsky, A. N, N. Vavra, and J. S. Porter. 2008. Sexual reproduction in gymnolaemate Bryozoa: history and perspectives of the research. Pp. 117-210, in P. N. Wyse Jackson and M. E. Spencer Jones, eds. Annals of bryozoology 2: aspects of the history of research on bryozoans, International Bryozoology Association, Dublin.
78. Packard, G. C., C. R. Tracy, and J. J. Roth. 1977. The physiological ecology of reptilian eggs and embryos, and the evolution of viviparity within the class Reptilia. Biol. Rev. 52:71-105.
79. Pires, M. N., R. D. Bassar, K. E. McBride, J. U. Regus, T. Jr. Garland, and D. N. Reznick. 2011. Why do placentas evolve? An evaluation of the life-history facilitation hypothesis in the fish genus Poeciliopsis. Funct. Ecol. 25:757-768.
80. Pollux, B. J. A., M. N. Pires, A. I. Banet, and D. N. Reznick. 2009. Evolution of placentas in the fish family Poeciliidae: an empirical study of macroevolution. Ann. Rev. Ecol. Evol. Syst. 40:271-289.
81. Reed, C. G. 1991. Bryozoa. Pp. 85-245. in A. C. Giese, J. S. Pearse and V. B. Pearse, eds. Reproduction of marine invertebrates. Vol. 6, Echinoderms and lophophorates. Boxwood Press, Pacific Grove, CA.
82. Reynolds, J. D., N. B. Goodwin, and R. P. Freckleton. 2002. Evolutionary transitions in parental care and live bearing in vertebrates. Proc. Roy. Soc. B 357:269-281.
83. Reznick, D. N., M. Mateos, and M. S. Springer. 2002. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298:1018-1020.
84. Reznick, D., R. Meredith, and B. B. Collette. 2007a. Independent evolution of complex life history adaptations in two families of fishes, live-bearing halfbeaks (Zenarchopteridae, Beloniformes) and Poeciliidae (Cyprinodontiformes). Evolution 61:2570-2583.
85. Reznick, D., T. Hrbek, S. Caura, J. De Greef, and D. Roff. 2007b. Life history of Xenodexia ctenolepis: implications for life history evolution in the family Poeciliidae. Biol. J. Linn. Soc. 92:77-85.
86. Rothchild, I. 2003. The yolkless egg and the evolution of eutharian viviparity. Biol. Repr. 68:337-357.
87. Santagata, S., and W.C. Banta. 1996. Origin of brooding and ovicells in cheilostome bryozoans: interpretive morphology of Scrupocellaria ferox. Invert. Biol. 115: 170-180.
88. Shine, R., and M. S. Y. Lee. 1999. A reanalysis of the evolution of viviparity and egg-guarding in squamate reptiles. Herpetologica. 55:538-549.
89. Silén, L. 1945. The main features of the development of the ovum, embryo and ooecium in the ooecioferous Bryozoa Gymnolaemata. Ark. Zool. 35A:1-34.
90. Stewart, J. R. 1992. Placental structure and nutritional provision to embryos in predominantly lecithotrophic viviparous reptiles. Amer. Zool. 32:303-312.
91. Stewart, J. R., and M. B. Thompson. 2000. Evolution of placentation among squamate reptiles: recent research and future directions. Comp. Biochem. Phys. A 127:411-431.
92. Swiderski, Z., and W. E. R. Xylander. 2000. Vitellocytes and vitellogenesis in cestodes in relation to embryonic development, egg production and life cycle. Int. J. Parasitol. 30:805-817.
93. Taylor, P. D., and F. K. McKinney. 2002. Brooding in the Cretaceous bryozoan Stichomicropora and the origin of ovicells in cheilostomes. Pp. 307-314 in P. N. Wyse Jackson, C. J. Buttler and M. E. Spencer Jones, eds. Bryozoan studies 2001. A. A. Balkema Publishers, Lisse, Tokyo.
94. Tompa, A. S. 1984. Land snails (Stylommatophora). Pp. 47-140 in K. M. Wilbur, A. S. Tompa, N. H. Verdonk and J. A. M. Van Den Biggelaar, eds. The Mollusca, Vol. 7, Reproduction. Academic Press, Orlando, San Diego, San Francisco, New York, London, Toronto, Montreal, Sydney, Tokyo, Sao Paulo.
95. Tsyganov-Bodounov, A., P. J. Hayward, J. S. Porter, and D. O. F. Skibinski ., 2009. Bayesian phylogenetics of Bryozoa. Mol. Phylogenet. Evol. 52:904-910.
96. Turner, C. L. 1940. Pseudoamnion, pseudochorion, and follicular pseudoplacenta in poeciliid fishes. J. Morphol. 67:59-89.
97. Waeschenbach, A., P. D. Taylor, and D. T. Littlewood. 2012. A molecular phylogeny of bryozoans. Mol. Phylogenet. Evol. 62:718-735.
98. Wagner, G. P., and V. J. Lynch. 2010. Evolutionary novelties. Curr. Biol. 20:R48-52.
99. Waters, A. W. 1913. The marine fauna of British East Africa and Zanzibar from collections made by Cyril Crossland. Bryozoa-Cheilostomata. Proc. Zool. Soc. London 83:458-537.
100. Weygoldt, P. 1969. The biology of pseudoscorpions. Harvard Univ. Press, Cambridge, MA.
101. Wooding, P., and G. Burton. 2008. Comparative placentation: structures, functions and evolution. Springer-Verlag, Berlin, Heidelberg.
102. Woollacott, R. M., and R. L. Zimmer 1972. A simplified placenta-like brooding system in Bugula neritina (Bryozoa). Pp. 30-31 in C. J. Arceneaux, ed. 30th Annual Proceedings of the Electron Microscope Society of America.Claitor's Publishing Division, Baton Rouge, LA.
103. Woollacott, R. M., and R. L. Zimmer. 1975. A simplified placenta-like system for the transport of extraembryonic nutrients during embryogenesis of Bugula neritina (Bryozoa). J. Morph. 147:355-378.
104. Wourms, J. P. 1981. Viviparity: the maternal-fetal relationships in fishes. Amer. Zool. 21:473-515.
105. Wourms, J. P., and J. Lombardi. 1992. Reflections on the evolution of piscine viviparity. Amer. Zool. 32:276-293.
106. Wourms, J. P., B. D. Grove, and J. Lombardi. 1988. The maternal-embryonic relationship in viviparous fishes. Pp. 1-134 in W. S. Hoar and D. J. Randall, eds. Fish physiology, Vol 11. Academic Press, New York.
107. Wray, G. A. 1995. Evolution of larvae and developmental modes. Pp. 413-447 in L. McEdwards, ed. Ecology of marine invertebrate larvae. CRC Press, Boca Raton, London, New York, Washington, DC.