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Unusual Pattern of Embryogenesis of Caryophyllia Inornata (Scleractinia, Caryophylliidae) in the Mediterranean Sea: Maybe Agamic Reproduction?

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Unusual Pattern of Embryogenesis of Caryophyllia Inornata (Scleractinia, Caryophylliidae) in the Mediterranean Sea: Maybe Agamic Reproduction? JOURNAL OF MORPHOLOGY 273:943–956 (2012) Unusual Pattern of Embryogenesis of Caryophyllia inornata (Scleractinia, Caryophylliidae) in the Mediterranean Sea: Maybe Agamic Reproduction? Stefano Goffredo,1* Chiara Marchini,1 Marta Rocchi,1 Valentina Airi,1 Erik Caroselli,1 Giuseppe Falini,2 Oren Levy,3 Zvy Dubinsky,3 and Francesco Zaccanti1 1Marine Science Group, Department of Evolutionary and Experimental Biology, Alma Mater Studiorum – University of Bologna, Bologna 40126, Italy 2Department of Chemistry ‘‘G. Ciamician’’, Alma Mater Studiorum – University of Bologna, Bologna 40126, Italy 3The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel ABSTRACT While knowledge of the reproductive biol- wide range of reproductive strategies of this group ogy of tropical scleractinian corals is extensive, informa- remains enigmatic (Loya and Sakai, 2008). Of the tion from temperate zones is limited. The aim of this more than 1,500 recognized coral species, charac- study is to describe the reproductive biology of Caryo- teristics of sexual reproduction have now been phyllia inornata, a temperate species, and to increase recorded in at least 444 species (Harrison, 2011) the understanding of the reproductive strategies of Med- iterranean corals. Samples of C. inornata were collected mainly from tropical and subtropical zones during SCUBA surveys at Elba island. Sexually active (Fadlallah, 1983; Heltzel and Babcock, 2002; Neves individuals displayed either male or female germ cells, and Pires, 2002; Mangubhai and Harrison, showing a gonochoric sexuality. C. inornata exhibited an 2008a,b). Information on scleractinians from tem- unusual pattern of embryogenesis. Embryos appeared perate zones, however, is limited (Szmant-Froelich throughout the whole year in males and in sexually et al., 1980; Beauchamp, 1993). Data on corals inactive individuals, and they did not show a seasonal from the Mediterranean Sea come from observa- pattern of development, as usually expected for sexual tions made more than a century ago by Lacaze- reproduction. This observation suggests the possibility of Duthiers (1873), a few observations on Cladocora asexual origin. These embryogenetic sexually inactive caespitosa (Kruzic et al., 2008) and recent studies individuals were larger in size than the embryogenetic sexually active ones, and they might be senile polyps on Balanophyllia europaea (Goffredo et al., 2002), that preserve the ability to produce embryos only by Leptopsammia pruvoti (Goffredo et al., 2005, agamic reproduction. J. Morphol. 273:943–956, 2006), and Astroides calycularis (Goffredo et al., 2012. Ó 2012 Wiley Periodicals, Inc. 2010, 2011). The variety of reproductive processes and modes KEY WORDS: embryo development; gametogenesis; among coral species partially reflects the extraor- sexual inactive polyps; sexuality; reproductive mode dinary ability of their cells to differentiate and to provide their tissues with increased plasticity and evolutionary adaptability (Campbell, 1974; Hol- stein et al., 2003; Harrison, 2011). The abundance INTRODUCTION Contract grant sponsor: European Research Council under the Knowledge of pattern of sexuality and mode of European Union’s Seventh Framework Programme (FP7/2007- 2013); Contract grant number: 249930-CoralWarm: Corals and reproduction are fundamental for the understand- global warming: the Mediterranean versus the Red Sea. Contract ing of the macroevolutionary processes of all multi- grant sponsors: Marine and Freshwater Science Group Association cellular organisms (Kerr et al., 2011). Knowledge (www.msgassociation.net) and the Ministry of Education, University of the reproductive biology of corals (Scleractinia), and Research (MIUR). gained by studying their sexuality (hermaphroditic *Correspondence to: Stefano Goffredo, Department of Evolution- or gonochoric), reproductive mode (broadcasting or ary and Experimental Biology, Alma Mater Studiorum—University brooding), embryonic (coeloblastula or stereoblas- of Bologna, Via Selmi 3, Bologna 40126, Italy. tula), and larval development (benthic or plank- E-mail: [email protected] tonic), is the first step to understanding the popu- lation dynamics of marine organisms (e.g., Gof- Received 16 January 2012; Revised 23 March 2012; fredo et al., 2005). Accepted 6 April 2012 Despite in-depth studies over the last three dec- Published online 18 June 2012 in ades, which have greatly increased understanding Wiley Online Library (wileyonlinelibrary.com) of the reproductive biology of scleractinians, the DOI: 10.1002/jmor.20039 Ó 2012 WILEY PERIODICALS, INC. 944 S. GOFFREDO ET AL. of information on the biology and reproductive event may allow for the rapid recolonization of ecology of scleractinians exceeds that of some other these areas by the localized recruitment of asex- groups of marine invertebrates and therefore pro- ually generated larvae from surviving colonies vides an important model for the understanding of (Sherman et al., 2006). Gilmour (2002a) observed their evolution and life cycles (Harrison, 2011). that the Australian population of the Fungia fun- Complex and sometimes controversial evolutionary gites coral, exposed to a high rate of chronic sedi- forces are the basis for sexual determination in mentation, shows up to 30% of asexually derived plants and animals. These may present the same polyps. The population of Fungia scutaria,common sex throughout their lifetime, or change from one in very rough shallow water, shows a more marked functional sex to another, displaying phenomena of asexual budding compared with populations of Fun- sexual inversion (Loya and Sakai, 2008). Reaching gia granulosa, common in calm, deep water, sug- sexual maturity depends on a balance between gesting that the evolution of distinct reproductive growth and risk of death, which is linked to the strategies in closely correlated species might in part age and size of the organisms. Variations in age be the consequence of different environmental con- and size at the first reproductive event and differ- straints (Kramarsky-Winter and Loya, 1998; Gof- ences in the ‘‘sex ratio’’ influence population fredo and Chadwick-Furman, 2003). growth rates (Fujiwara and Caswell, 2001). These Changes in several biological processes, for variations are important, as they may represent example, the consequences of climate changes, are the beginning of evolutionary divergences (Rich- already evident in several ecosystems (Harley mond and Hunter, 1990). et al., 2006). Increases in temperature may cause Various studies performed in the 1970s and alterations in gamete release into the environment 1980s showed that in several ovoviviparous antho- (Lawrence and Soame, 2004), as well as in the zoa planulae production can be derived by asexual quality of the eggs and survival of the larvae reproductive processes (Ottaway and Kirby, 1975; (McClanahan et al., 2009; Randall and Szmant, Black and Johnson, 1979; Stoddart, 1983; Ayre 2009). The repercussions of climate change are and Resing, 1986), contradicting the assumption expected to be greater in the temperate and high- that these are only of sexual origin (Hyman, 1940; latitude zones (Solomon et al., 2007), with marked Connell, 1973). The selective advantages of sexual consequences in organisms that display seasonal- versus asexual reproduction change in different ity in gonadic development (Lawrence and Soame, conditions, and the energy allocation intended for 2004). Therefore, sexual reproductive processes are each reproductive strategy can reflect changes in sensitive to a wide range of natural and anthropo- the environment (Bradshaw, 1965; Jackson and genic stress factors, which impair or block the crit- Coates, 1986; Stearns, 1992). Reproductive flexibil- ically important phases of reproduction and ity and its effect on the structure of the population recruitment required to maintain and replenish are often generalized in life-history theory. Theo- coral populations (Harrison, 2011). Without sexual retical models suggest under favorable conditions recombination, these populations have little and low stress levels, energy investment in asex- chance of adapting to changes in environmental ual propagation predominates (Williams and Mit- conditions and, in particular, ocean warming (van ton, 1973; Warner, 1975; Williams, 1975). Such Woesik, 2009). Considering that the reproduction asexual reproduction would generate a clonal line of coral seems more sensitive to stress in compari- that might contribute to keeping populations son with other vital functions (Harrison and Wal- inside the area of the parental habitat, thus propa- lace, 1990), the presence of ecologically appropriate gating well-adapted genotypes at the local level. environmental conditions is essential to ensure On the other hand, when local conditions are reproductive success (Harrison, 2011). unfavorable and stress levels are high, more This study, which is part of the European project energy will be invested in sexual reproduction and FP7-IDEAS ERC ‘‘Corals and global warming: the dispersion (Warner, 1975; Williams, 1975; Car- Mediterranean versus the Red Sea,’’ aims to inves- valho, 1994). This produces a genotypically differ- tigate the reproduction of Caryophyllia inornata ent lineage, which might enable a wide dispersion (Fig. 1) in the northern Tyrrhenian Sea to increase or recolonization of more heterogeneous habitats knowledge on Mediterranean scleractinian corals, (Williams, 1975; Maynard Smith, 1978), thus con- key
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