Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond?

Integrative and Comparative Biology, Oct 2006 by Pearson, Gareth A, Serr�o, Ester A

Synopsis

In the marine environment, both external fertilization and settlement are critical processes linking adult and early juvenile life-history phases. The success of both processes can be tightly linked in organisms lacking a larval dispersive phase. This review focuses on synchronous gamete release (= spawning) in fucoid algae. These brown macroalgae are important components of temperate intertidal ecosystems in many parts of the world, and achieve synchronous gamete release by integrating various environmental signals. Photosynthesis-dependent sensing of boundary-layer inorganic carbon fluxes, as well as blue light and green light signals, possibly perceived via a chloroplast-located photoreceptor(s), are integrated into pathways that restrict gamete release to periods of low water motion. Avoidance of turbulent and/or high flow conditions in the intertidal zone allows high levels of fertilization success in this group. Temporal patterns and synchrony of spawning in natural populations are reviewed. Most species/populations have a more or less semilunar periodicity, although phase differences occur both between and within species at different geographical locations, raising the possibility that tidal and diurnal cues are more important than semilunar cues in entraining the response. The ecological and evolutionary role(s) of synchronous spawning in the intertidal zone are considered, particularly with regard to hybridization/reproductive isolation in species complexes, and reproductive versus recruitment assurance in the intertidal zone, where synchronous spawning during calm periods may be important for recruitment assurance in addition to fertilization success. Ways in which the roles of spawning synchrony could be tested in closely related species with contrasting mating systems (outcrossing versus selfing) are discussed.

Introduction

Broadcast spawning and external fertilization are common in many groups of marine organisms, despite the pitfalls of ensuring reproductive success in the sea. Perhaps the single most important factor favoring successful syngamy is the synchronous release of gametes from reproductive individuals. Indeed, the literature contains many striking examples of spawning synchrony, from the Palolo worm in the south Pacific (see Gaspers 1984) to the mass spawning of many species of corals (Harrison and others 1984; Babcock and others 1986). In these and other examples, organisms respond to 1 or more cues from multiple environmental cycles, including daily (light-dark), tidal, semilunar, lunar, and seasonal, to synchronize gamete release (Morgan and Christy 1994; Yamahira 2004; Skov and others 2005). Tight control over the timing of gamete release, and therefore sensitivity to environmental cues, is very important for reproductive assurance in externally fertilizing species. Until recently, the prevailing paradigm has been that sperm limitation is widespread in the sea (reviewed by Levitan and Petersen 1995; but also see Yund 2000). This conclusion is mainly based on experimental studies of induced spawning (for example, Pennington 1985; Levitan and others 1992) and theoretical considerations of the effects of turbulent flow regimes on gamete dilution rates in the water column (Denny and Shibata 1989). However, this view has increasingly come under scrutiny because of studies of natural spawning events, primarily in fucoid algae, in which fertilization rates close to 100% are typical for several species (Brawley 1992; Pearson and Brawley 1996; Serr�o and others 1996; Berndt and others 2002; Ladah and others 2003). Similarly, realistic time-integrated spawning patterns, using non-manipulated gametes and ecologically relevant flow rates, may modify the current view of broadcast spawning as a purely water column process (Yund and Meidel 2003).

Following syngamy, many of the most-studied broadcast-spawning invertebrates undergo a larval dispersal phase. In contrast, for fucoids and other species with direct development, spawning/fertilization and settlement/recruitment processes are tightly coupled. Variation in dispersal scales in the marine environment (Kinlan and Gaines 2003; Palumbi 2004) may thus be partially linked to life-history processes and constraints. Furthermore, the steep environmental gradients within the intertidal zone, and the narrow vertical ranges of many species, may confer fitness benefits on individuals that restrict dispersal. Long-distance dispersal of gametes or zygotes may result more in wastage of zygotes than in effective gene flow for species with fringe-like intertidal distributions and direct development, and for which long-distance dispersal may be mediated by other means (for example, via the transport of dislodged reproductive adult individuals in drift material). Thus, synchronous release of gametes can be critical for recruitment assurance in addition to reproductive assurance. Although tightly linked processes, we will argue that the relative importance of spawning synchrony for reproduction and recruitment might be dissected using fucoid models in which sympatric species have different reproductive modes, as well as different mating systems (hermaphroditic and selfing versus dioecious and outcrossing) (Engel and others 2005). This is possible because the predicted importance of synchrony for reproductive assurance, but not recruitment assurance, varies with mating system. The genus Fucus contains sibling species that occur in sympatry throughout much of their respective ranges. Asynchrony between species and synchrony within species may be under strong selection to reinforce prezygotic reproductive isolation and reduce the likelihood of hybridization (Gardner 1997; Fukami and others 2003; Levitan and others 2004).