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. franksi, 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.

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

“…Reciprocal transplantation suggests divergence between colonies found at different depths is adaptive and selection is strong enough to maintain the separation of the two lineages at the ends of the depth gradient. This divergent selection may by itself result in reproductive isolation via immigrant inviability (poor performance and viability of larvae settling at the wrong depth) and temporal isolation (spawning at different times) (29). We suggest divergence between Shallow and Deep lineages of E. flexuosa is driven by adaptation to different conditions at different depths (1), facilitated by developmental plasticity (30,31) and prolonged opportunity for depth-specific selection before reproduction.…”

“…Divergent selection along depth gradients is generated by associated factors such as the quantity and quality of light, the force of waves and currents, sediment load, the distribution of predators and mutualists, and the availability and composition of food. In response to this variation in environmental conditions, closely related species or populations found at different depths have been found to differ in their morphologies (5, 13), feeding strategies (32,33), metabolic rates (33), symbiotic relationships (34), resistance to predators (35), and spawning times (16,29). In E. flexuosa's close relative Plexaura homomalla (Eunicea and Plexaura are paraphyletic), depth-segregated sister species increase heterotrophy and decrease photosynthesis as depth increases (32).…”

“…As for flowering plants segregated by altitude (41,55), marine broadcasters segregated by depth often differ in their time of spawning, decreasing the probability of cross-fertilization between depth-segregated colonies (16,29). Before spawning events, colonies in deep areas of E. flexuosa lack mature eggs compared with shallow ones (22).…”

The clock gene cryptochrome of Bactrocera cucurbitae (Diptera: Tephritidae) in strains with different mating times

“…In the wild, temporal reproductive isolation results from differences in mating season in birds (Friesen et al, 2007), mating period in insects (Bush, 1969;Hendry et al, 2000), timing of gamete release in corals (Levitan et al, 2004), timing of migration and breeding in fishes , and time of mating in flies .…”

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“…High fertilization success is also observed under natural conditions (Levitan et al 2004). While pre-and post-settlement mortality remains among the main potential causes, it is also possible that the effects of climate change in the Caribbean may have disrupted ecological interactions required for the recruitment process itself (Harrison 1990), specifically the interaction between coral larvae and natural settlement cues.…”