Vol. 378: 113–124, 2009 MARINE ECOLOGY PROGRESS SERIES Published March 12 doi: 10.3354/meps07850 Mar Ecol Prog Ser Independent evolution of matrotrophy in the major classes of Bryozoa: transitions among reproductive patterns and their ecological background Andrew N. Ostrovsky1, 4,*, Dennis P. Gordon2, Scott Lidgard3 1Department of Invertebrate Zoology, Faculty of Biology & Soil Science, St. Petersburg State University, Universitetskaja nab. 7/9, 199034, St. Petersburg, Russia 2National Institute of Water & Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, New Zealand 3Department of Geology, Field Museum of Natural History, 1400 S. Lake Shore Dr., Chicago, Illinois 60605, USA 4Present address: Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria ABSTRACT: Bryozoa are unique among invertebrates in possessing placenta-like analogues and exhibiting extraembryonic nutrition in all high-level (class) taxa. Extant representatives of the classes Stenolaemata and Phylactolaemata are evidently all placental. Within the Gymnolaemata, placenta- like systems have been known since the 1910s in a few species, but are herein reported to be wide- spread within this class. Placental forms include both viviparous species, in which embryonic devel- opment occurs within the maternal body cavity, and brooding species, in which development proceeds outside the body cavity. We have also identified an unknown reproductive pattern involv- ing macrolecithal oogenesis and placental nutrition from a new, taxonomically extensive anatomical study of 120 species in 92 genera and 48 families of the gymnolaemate order Cheilostomata. Results support the hypothesis of evolution of oogenesis and placentation among Cheilostomata from oligolecithal to macrolecithal oogenesis, followed by brooding, through incipient matrotrophy com- bining macrolecithal oogenesis and placentation, to oligolecithal oogenesis with subsequent placen- tal brooding. The distribution of reproductive patterns within the phylum suggests that variations of placentation evolved in all 3 bryozoan classes, and possibly several times within both gymnolaemate orders. We infer that extraembryonic nutrition may be advantageous to species through enhanced developmental plasticity, and, in fast-growing ephemeral colonies, simultaneous volumetric growth and embryonic development may facilitate earlier larval release and occupation of vacant space. KEY WORDS: Matrotrophy · Placenta · Reproductive patterns · Evolution · Bryozoa Resale or republication not permitted without written consent of the publisher INTRODUCTION centation, involving intimate contact or even fusion of the fetal and parental tissues and ‘nutrient transfer via Matrotrophy, or extraembryonic nutrition (EEN), is cell secretions or blood constituents’ to the embryo or considered the most complex nutritional relationship its enclosing space (Crespi & Semeniuk 2004, p. 638). between a parent and an embryo, enhancing off- The distribution of matrotrophy in the Eumetazoa is spring fitness under certain circumstances (Wourms strikingly scattered. Basically, a few species in some & Lombardi 1992, Mousseau & Fox 1998, Trexler & genera or families within a class or phylum exhibit DeAngelis 2003, Marshall & Uller 2007). It occurs in matrotrophy, whereas the others lack it. For instance, both viviparous and some brooding animals by a vari- nutrient transfer from the maternal organism to the ety of methods (oophagy, adelphophagy, histophagy, embryo is known in 1 scyphozoan jellyfish, a few ces- placental nutrition). The most complex variant is pla- tode flatworms, a polychaete, several species of gas- *Email: [email protected] © Inter-Research 2009 · www.int-res.com 114 Mar Ecol Prog Ser 378: 113–124, 2009 tropods and of bivalve molluscs, 2 kamptozoans, and reproductive patterns have occurred repeatedly among 3 echinoderms. Matrotrophy is more common within gymnolaemate lineages. We also offer some provi- the Arthropoda, in which EEN is characteristic of 2 sional ecological considerations based on our survey, families of scorpions, several isopod crustaceans, some increasing awareness of the importance of maternal genera in a few orders of insects, and 2 genera of provisioning among marine animals, and recent eco- mites. It is also found in 2 families of Onychophora, 2 logical studies of cheilostome bryozoans. species of Ascidiacea, numerous families of elasmo- branch and bony fishes, and in some amphibians and reptiles. Most species in these groups are either MATERIALS AND METHODS oviparous or viviparous, but not matrotrophic (Giese & Pearse 1974, 1975a,b, 1977, Giese et al. 1979, 1987, Specimens were collected by various methods and 1991, Wourms et al. 1988, Adiyodi & Adiyodi 1989, fixed either in 2.5% glutaraldehyde (buffered in 1990, Blackburn 1992, Charmantier & Charmantier- 0.1 M Na-cacodylate with 10.26% sucrose, pH 7.3) or Daures 1994, Schwartz & Dimock 2001, Crespi & Bouin’s fluid without acetic acid. While still in fixative Semeniuk 2004, Korneva 2005, von Rintelen & Glaub- they were decalcified for 6 to 12 h using a few drops of a recht 2005, Glaubrecht et al. 2006, Koya & Munoz 2 N solution of hydrochloric acid; gradually dehydrated 2007, Reznick et al. 2007). Exceptions to patchy dis- in an ethanol series (40–50–60–70–80–90–96%), em- tribution of EEN are the Pseudoscorpionida, Salpida bedded in plastic (epoxy resin type TAAB 812), sec- (Tunicata), and placental mammals, in which it occurs tioned (1.0 µm thick) with a glass knife, and stained in all species (Weygoldt 1969, Bone 1998, Lombardi with Richardson’s stain (1% water solution of methyl- 1998, Mess & Carter 2007). ene blue, Na-tetraborate and azur II, mixed in propor- The phylum Bryozoa, all species of which are colonial tions 1:1:2) using standard methods (Richardson et al. suspension feeders, is an exception too, as we report 1960). Sections were observed and digital images were below. All extant species of the class Stenolaemata (or- made with Nikon 104 and Nikon 118 FXA dissecting der Cyclostomata) are viviparous, possessing special- light microscopes. ized nutritive tissue and embryos that are incubated Altogether, sections of 120 species belonging to 92 intracoelomically in characteristic brooding zooids genera and 48 families of the gymnolaemate order (gonozooids) (Harmer 1893, 1896, 1898, Borg 1926). In- Cheilostomata were prepared and studied (Table 1). sofar as these gonozooids are known in fossil cyclo- Our criteria for recognizing extraembryonic nutrition stomes (Taylor & Michalik 1991, Lidgard et al. 1993), include comparing the size of the zygotes/early em- matrotrophy is inferred to have existed in this order at bryos and late embryos/larvae, and/or comparing the least since the Late Triassic. Similarly, all species of the epithelial lining of empty and incubating brood cham- class Phylactolaemata studied so far have EEN by ei- bers, since EEN is mediated via the hypertrophied ther spot- or ring-like placental analogues, developing epithelial cells (embryophore) that develop inside inside a brooding sac the cavity of which is external rel- these chambers (Fig. 1). Simultaneously anatomical ative to the maternal body cavity (Braem 1890, Brien study of oogenesis was undertaken aiming to recog- 1953). In Gymnolaemata, the largest bryozoan class nize the type and numbers of oocytes. with >1000 genera, matrotrophy was, until recently, known only in relatively few taxa — in the viviparous family Epistomiidae (genera Epistomia, Synnotum) and RESULTS in the families Bugulidae (Bicellariella, Bugula), Candi- dae (Scrupocellaria), and Hippothoidae (Celleporella). Anatomical data These taxa are among the majority of gymnolaemates that brood their embryos in extrazooidal incubation In addition to the above-mentioned taxa, we found chambers (ovicells) (Marcus 1938, 1941, Woollacott & EEN in the families Flustridae (genera Gregarinidra, Zimmer 1972, 1975, Dyrynda 1981, Dyrynda & King Isosecuriflustra, Klugeflustra), Beaniidae (Beania), 1982, 1983, Dyrynda & Ryland 1982, Hughes 1987, Cellariidae (Cellaria), Microporidae (Micropora), Crib- Santagata & Banta 1996, Ostrovsky 1998). rilinidae (Figularia), Catenicellidae (Costaticella, Crib- We report here the results of an extensive light- ricellina, Pterocella), Watersiporidae (Watersipora), microscopic anatomical study, revealing that EEN is Lanceoporidae (Calyptotheca), Myriaporidae (Myria- far more common in gymnolaemates than previously pora), and Urceoliporidae (Reciprocus, Urceolipora). realized. The results point out seemingly independent Placental analogues are represented structurally appearances of matrotrophy. To the extent that broad by hypertrophied epithelial cells (embryophore) of similarities — and independent acquisition — evidenced the maternal body wall transporting nutrients to the in these cases hold true, they imply that transitions in brooding cavity by exocytosis in Cheilostomata. In its Ostrovsky et al.: Matrotrophy in Bryozoa 115 Fig. 1. Longitudinal sections through brood chambers with placental analogues in 3 cheilostome bryozoans (light microscopy). (A,B) Bugula flabellata (Bugulidae) (Pattern III): (A) ovicell with an oligolecithal zygote and non-developed embryophore and (B) partly grown embryo and fully developed embryophore. (C) Ovicell of Myriapora truncata (Myriozoidae) with an embryophore and macrolecithal zygote (Pattern IV). (D) Internal brood sac of Reciprocus regalis