Copper reduces fertilisation success and exacerbates Allee effects in the field

Hollows, Cam F.; Johnston, Emma L.; Marshall, Dustin J.

doi:10.3354/meps333051

Cited by 42 publications

(37 citation statements)

References 47 publications

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“…In externally fertilising species (such as most fish, amphibians and marine invertebrates), however, sperm are shed into a highly variable, uncontrolled environment where individual spermatozoa, both among and within ejaculates, can experience vastly different conditions. For example, externally shed sperm can be exposed to waterborne pollutants (Hollows et al, 2007), variable thermal regimes (Bownds et al, 2010) and very different hydrodynamic conditions (Mead and Denny, 1995). Whether this massive variation in the sperm environment generates differences in the phenotype of the offspring these sperm go on produce remains largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Ritchie

Marshall

2013

Journal of Experimental Biology

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SUMMARYFor organisms with complex life histories, the direction and magnitude of phenotypic links among life-history stages can have important ecological and evolutionary effects. While the phenotypic links between mothers and offspring, as well as between larvae and adults, are well recognised, the links between sperm phenotype and offspring phenotype have been less well explored. Here, we used a split-clutch/split-ejaculate design to examine whether the environment that sperm experience affects the subsequent performance of larvae in the broadcast spawning marine invertebrate Galeolaria gemineoa. The environment that sperm experienced affected the developmental success of larvae sired by these sperm; larvae sired by sperm that experienced low salinities had poorer developmental success than larvae sired by sperm that experienced a normal salinity. When we explored the interactive effects of the sperm environment and the larval environment with an orthogonal design, we found an interaction; when sperm and larvae experienced the same environment, performance was generally higher than when the sperm and larval environments differed. These effects could be due to selection on specific sperm phenotypes, phenotypic modification of the sperm or both. Together, our results challenge the traditional notion that sperm are merely transporters of genetic material; instead, significant covariance between sperm and offspring phenotypes exists. Our study adds to a growing list that demonstrates that fertilisation does have a homogenising effect on the phenotype of the zygote, and that events before fertilisation during the gamete phase can carry through to affect performance in later life-history stages.

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Section: Introductionmentioning

confidence: 99%

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Ritchie

Marshall

2013

Journal of Experimental Biology

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“…Based on these trials, we used 10 4 cells ml 21 as our low density and 10 5 cells ml 21 as our high one. These densities fall within the continuum available to Galeolaria eggs in the field, and fertility at our low density is comparable with field estimates [41]. We collected each male's ejaculate (reserving 10 ml for sperm phenotyping; see below) and recorded its initial sperm density (10 6 -10 8 cells ml…”

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confidence: 99%

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

Monro¹,

Marshall²

2016

Proc. R. Soc. B.

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Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

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“…Similarly, sperm attachment can continue for up to 5·min after fertilisation in other taxa (Gould and Stephano, 2003;Wong and Wessel, 2006). The density of adult Galeolaria caespitosa varies dramatically in the field and so it is difficult to predict the typical sperm environment for eggs of this species, but a recent manipulative study suggests that concentrations in the field will be limiting (Hollows et al, 2007). That the onset of the permanent polyspermy block is rapid further supports the notion that sperm are limiting in the field and there is strong selection pressure to reduce the number of sperm that are 'wasted' by fertilised eggs.…”

Section: Discussionmentioning

confidence: 99%

Sperm release strategies in marine broadcast spawners: the costs of releasing sperm quickly

Marshall

Bolton

2007

Journal of Experimental Biology

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SUMMARY When under competition for fertilisations, males are thought to increase their reproductive success by releasing as many sperm as possible into the reproductive arena and in many species, this prediction holds. For marine invertebrates, which utilise the ancestral strategy of broadcast spawning eggs and sperm, however, it appears that males tend to release their sperm more slowly than females release their eggs. Marine invertebrate eggs typically have a relatively slow permanent block to polyspermy (whereby eggs become impermeable to further sperm attachment), and for several minutes after fertilisation, sperm can continue to attach to a fertilised egg. We hypothesised that releasing sperm slowly minimises the `wastage' of sperm on already fertilised eggs. We simulated different sperm release rates in a flume using the broadcast spawning polychaete, Galeolaria caespitosa. Sperm release rates strongly affected overall fertilisation success: higher release rates resulted in lower fertilisation rates. Laboratory studies confirmed that the `permanent' block to polyspermy in G. caespitosa took less than a minute to form but this lag was sufficient to result in some sperm wastage. Thus upstream, fertilised eggs that have not formed a permanent block to polyspermy can remove sperm from the pool that would otherwise fertilise downstream sibling eggs. We suggest that while electrical blocks to polyspermy evolved in response to excess sperm, permanent blocks to polyspermy could have evolved in response to sperm limitation (insufficient sperm).

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Copper reduces fertilisation success and exacerbates Allee effects in the field

Cited by 42 publications

References 47 publications

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

Sperm release strategies in marine broadcast spawners: the costs of releasing sperm quickly

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