In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate

Marshall, Dustin J.

doi:10.3354/meps236113

Cited by 70 publications

(104 citation statements)

References 21 publications

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“…This may in turn have wider implications for postsettlement survival of offspring. Some ascidians spawn in conditions that promote gamete and larval retention (58)(59)(60) and are therefore unlikely to disperse far from their natal habitat. This means that in addition to being a good predictor of the sperm environment, local density may also be a good predictor of offspring environment.…”

Section: Discussionmentioning

confidence: 99%

Gamete plasticity in a broadcast spawning marine invertebrate

Crean

Marshall

2008

Proc. Natl. Acad. Sci. U.S.A.

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Sperm competition has classically been thought to maintain anisogamy (large eggs and smaller sperm) because males are thought to maximize their chance of winning fertilizations by trading sperm size for number. More recently it has been recognized that sperm quality (e.g., size, velocity) can also influence sperm competition, although studies have yielded conflicting results. Because sex evolved in the sea, debate has continued over the role of sperm competition and sperm environment in determining both sperm and egg size in externally fertilizing broadcast spawners. Remarkably, however, there have been no direct tests of whether broadcast spawners change the traits of their gametes depending on the likelihood of sperm competition. We manipulated the density (and thus, sperm environment) of a broadcast spawning ascidian (Styela plicata) in the field and then determined whether the phenotype of eggs and sperm changed. We found that sperm from adults kept at high density were larger and more motile than sperm from low-density adults. In vitro fertilizations revealed that sperm from high-density adults also lived longer and induced less polyspermy. Adult density also affected egg traits: eggs from high-density adults were smaller targets for sperm overall but produced larger ovicells than eggs from low-density adults. This suggests that broadcast spawning mothers balance (potentially conflicting) pre-and postzygotic selection pressures on egg size. Overall, our results suggest that sperm competition does not represent a strong force maintaining anisogamy in broadcast spawners. Instead, sperm limitation seems to select for large eggs and smaller, more numerous sperm.anisogamy ͉ sperm competition ͉ adaptive maternal effect ͉ transgenerational plasticity T he fundamental difference between the sexes is that males produce numerous, tiny sperm, and females produce relatively fewer, large eggs (anisogamy). Classic theory suggests that anisogamy most likely evolved by, and is maintained through, sperm competition (whereby sperm from 2 or more males compete to fertilize an egg) because males producing a greater number of sperm have a competitive advantage (refs. 1 and 2; but see ref. 3 for an alternative). In species with internal fertilization, competition for fertilizations can therefore be viewed as a ''raffle,'' whereby males that have the highest representation of sperm in the pool have the greatest chance of fertilizing eggs (4, 5). More recently, however, it has been proposed that sperm quality (e.g., sperm size, velocity, and longevity) can also influence the outcome of sperm competition (6, 7). Furthermore, because a male's sperm supply is limited (8, 9) and each mating opportunity may carry a variable risk of sperm competition (10), males must make decisions on the optimal allocation of both sperm number and quality for each mating event. The optimal allocation of sperm size and number within an ejaculate remains a source of intense debate (reviewed in refs. 7 and 9).The prediction that males should increase the ...

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Section: Discussionmentioning

confidence: 99%

Gamete plasticity in a broadcast spawning marine invertebrate

Crean

Marshall

2008

Proc. Natl. Acad. Sci. U.S.A.

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“…Many investigators have suggested sperm limitation as an ultimate cause for species with external fertilization (e.g. Marshall 2002). Besides a limited amount of water to dilute sperm, the extent of water agitation may be another factor, since the habitat at the collection site is isolated from wave action at low tide.…”

Section: Discussionmentioning

confidence: 99%

“…Direct observation in the field provides good evidence of natural spawning events, but systematic observation requires significant time and resources (see Harrison et al 1984, Himmelman et al 2008. Even in the intertidal zone, the most accessible marine environment, knowledge of a species' spawning times is often based on sporadic observations or indirect inferences from experiments (Marshall 2002, Pearson et al 2004.…”

Section: Resale or Republication Not Permitted Without Written Consenmentioning

confidence: 99%

Spawning time of two shallow-water brittle stars

Soong¹,

Lin²,

Chao³

et al. 2009

Mar. Ecol. Prog. Ser.

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“…However, fertilization in broadcast-spawning inverte-brates is influenced by a wider suite of processes than just those that control mixing of gametes in the water column. Spawn is viscous (Thomas 1994a) and can be retained on animals, where fertilization may occur as eggs are released (Svane & Havenhand 1993, Marshall 2002,Yund & Meidel 2003, or within clouds or strings of sperm formed on the surface of a spawning male. Experimental evidence indicates that in some taxa that project above the substrate, fertilization can take place on the surface of spawning animals and within the turbulent wake formed behind these animals; gametes may also sink to the substrate where fertilization occurs.…”

Section: Introductionmentioning

confidence: 99%

“…However, gametes can be retained on the surface of an animal for long periods of time (Svane & Havenhand 1993, Marshall 2002 and form clumps or strings that float in the water column, thus releasing eggs or sperm over time (Thomas 1994a). This retention can result in fertilizations occurring over a relatively long time frame (Yund & Meidel 2003).…”

Section: Introductionmentioning

confidence: 99%

Fertilization in a sea urchin is not only a water column process: effects of water flow on fertilization near a spawing female

Thomas

Kregting

Badgley

et al. 2013

Mar. Ecol. Prog. Ser.

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Fertilization efficiency in free-spawning invertebrates in the marine environment depends on the complex interaction between biological and physical factors. Experimental evidence indicates that in some taxa, a considerable amount of fertilization may take place on the substrate and within flow structures in close proximity to a spawning female. Gametes can be retained on a spawning animal, resulting in their slow release over relatively long periods of time, and retained eggs can be fertilized before they are released into the water column. Hydrodynamic conditions are likely to influence both the retention of gametes and their subsequent mixing in the water column as well as the relative importance of fertilization in the water column and in other locations near spawning animals. Here, fertilization in the broadcast-spawning sea urchin Strongylocentrotus droebachiensis was explored over a range of flow velocities (u-= 2 to 15 cm s −1 ) to determine the effect of velocity on fertilization and the relative contribution of different locations (aboral surface of the female, water column, wake, and the substrate behind the female) to overall fertilization. As velocity increased, the percentage of eggs fertilized declined in all locations. At all velocities, more eggs were fertilized on the aboral surface than in the water column. Further, as velocity increased, the relative contribution of the aboral surface to overall fertilization increased. These results highlight the importance of considering the interaction of hydrodynamics, organism morphology, and gamete properties in studies of fertilization in broadcast-spawning invertebrates.

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In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate

Cited by 70 publications

References 21 publications

Gamete plasticity in a broadcast spawning marine invertebrate

Gamete plasticity in a broadcast spawning marine invertebrate

Spawning time of two shallow-water brittle stars

Fertilization in a sea urchin is not only a water column process: effects of water flow on fertilization near a spawing female

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