Mechanisms of Reproductive Isolation Among Sympatric Broadcast-Spawning Corals of the Montastraea Annularis Species Complex

Abstract

Abstract.•Many coral species spawn simultaneously and have compatible gametes, leading to controversy over the nature of species boundaries and the frequency with which hybridization occurs. Three western Atlantic corals, Montastraea annularis, M. faveolata, and M. franks i, typify this controversy; they all spawn sympatrically on the same evenings after the fall full moons. Here we show, in both Panama and the Bahamas for multiple years, how a variety of mechanisms may act in concert to reproductively isolate all three species. Field studies indicate that M. franksi spawns two hours earlier than the other two species, and the eggs released during this earlier period disperse an average of 500 m by the time the other species spawn. Field measures of fertilization indicate that peak fertilization occurs when spawning synchrony is high and that corals that spawn at the tails of the spawning distributions have greatly reduced fertilization success. Laboratory studies indicate that there is a gametic incompatibility between M. faveolata and the other two species. There are regional differences in the gametic compatibility of M. franksi and M. annularis. In Panama, the two species are completely compatible, whereas in the Bahamas, M. franksi sperm can fertilize M. annularis eggs but the reciprocal cross often fails. Gamete age influences patterns of fertilization, such that very young eggs seem resistant to fertilization and old sperm lose viability after two hours. In sum, the combination of temporal differences in spawning, sperm aging, gamete dispersal and dilution, and gametic incompatibility act in various combinations among the three species, making it unlikely that hybrid fertilization would occur.

Fertilization Strategies

“…We have collated many of the key papers that refer to hard substratum species, and classify these here according to the different factors that have been identified as influencing fertilization success of hard substratum species (Table 10.1 ). Rothschild and Swann (1951) , Vogel et al (1982) , Destombe et al (1990), Levitan et al (1991) , Levitan (1993Levitan ( , 2000 , Manríquez et al (2001) , Powell et al (2001), Kupriyanova and Havenhand (2002) , Johnson and Yund (2004) , Levitan et al (2004) , Hodgson et al (2007), Muhlin et al (2008 Size Podolsky (2004) Egg Accessory structures (jelly coat, follicle cells, etc.) Lambert and Lambert (1981), Buckland-Nicks (1993), Farley andLevitan (2001), Levitan and Irvine (2001) , Podolsky (2001Podolsky ( , 2002Podolsky ( , 2004 , Villa and Patricolo (2001) Chemotaxis, chemokinesis Miller (1975Miller ( , 1985 , Maier and Müller (1986 , review), …”

“…Synchrony on broader scale may occur as a response to single or combinations of environmental signals such as lunar or tidal phases (e.g. Counihan et al 2001 ;Levitan et al 2004) , hydrodynamics (e.g. Serrão et al 1996b) , temperature (e.g.…”

“…Multi-species spawning synchrony (and resultant fertilization success) is, however, perhaps best known for corals (e.g. Levitan et al 2004 ;Guest et al 2005) . Despite widespread correlations between spawning and various possible environmental cues, particularly with lunar cycles (for many taxa throughout the world), the physiological mechanisms behind such patterns are poorly understood (but see Pearson and Brawley 1998;Pearson et al 2004 ;Guest 2008 and references therein).…”

“…Several recently diverged rocky shore species appear to have undergone incomplete reproductive isolation and still hybridize occasionally (e.g. brown algae, Coyer et al 2002 ;Engel et al 2005 ;sea urchins, Levitan 2002b ;bivalves, Bierne et al 2002 ;Beaumont et al 2004 ;corals, Vollmer and Palumbi 2002 ;Levitan et al 2004) . Speciation/hybridization processes trade-off under sperm-limiting conditions: specialization of gamete recognition proteins reduces risk of hybridization but may simultaneously reduce success of intraspecific fertilizations.…”

Coral mass spawning predicted by rapid seasonal rise in ocean temperature

“…Synchronized release of gametes for external fertilization in the water column is common among marine invertebrates with a sessile adult stage [11]; presumably because fertilization success is greatly diminished when small numbers of colonies spawn because of rapid gamete dilution in the water column [12,13]. Mass reproductive events, where multiple species release gametes or propagules simultaneously, are hypothesized to offer additional benefits, such as predator satiation [14,15].…”