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Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents.

Tunnicliffe V, St Germain C, Hilário A - PLoS ONE (2014)

Bottom Line: This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment.Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms.This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Victoria, Victoria, British Columbia, Canada; School of Earth & Ocean Sciences, University of Victoria, Victoria, British Columbia, Canada.

ABSTRACT
We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a "short-fat" phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

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Estimate of gonad extent with increasing size.The majority of animals in our initial samples were small with little gonad development in both sexes (open symbols). Each measure of gonad area is the mean of 10 cross-sections equidistant along the trunk. Several worms from the 2009 study (filled symbols) augment numbers of larger individuals to illustrate gonad extent in full maturity.
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pone-0110578-g004: Estimate of gonad extent with increasing size.The majority of animals in our initial samples were small with little gonad development in both sexes (open symbols). Each measure of gonad area is the mean of 10 cross-sections equidistant along the trunk. Several worms from the 2009 study (filled symbols) augment numbers of larger individuals to illustrate gonad extent in full maturity.

Mentions: We examined trophosome, gonad extent and gamete formation (Table 1) with onset of reproductive maturity in smaller animals. In 19 of 43 females and in 16 of 51 males, no gametes were seen in the sections; not until over 4 mm diameter did a majority of the females have oocytes when gonad began to enlarge. Only four individuals were over 7.5 mm diameter in this sample set but comparison with R. piscesae from the 2009 collection shows at larger sizes (over 10 mm vestimentum diameter) there is a marked increase in gonad extent, most notable in males (Figure 4). Trophosome area increased variably with vestimentum size (Spearman r = 0.58, p<0.01) to a maximum of 50% of the body area; there was no significant correlation with gonad size.


Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents.

Tunnicliffe V, St Germain C, Hilário A - PLoS ONE (2014)

Estimate of gonad extent with increasing size.The majority of animals in our initial samples were small with little gonad development in both sexes (open symbols). Each measure of gonad area is the mean of 10 cross-sections equidistant along the trunk. Several worms from the 2009 study (filled symbols) augment numbers of larger individuals to illustrate gonad extent in full maturity.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4206443&req=5

pone-0110578-g004: Estimate of gonad extent with increasing size.The majority of animals in our initial samples were small with little gonad development in both sexes (open symbols). Each measure of gonad area is the mean of 10 cross-sections equidistant along the trunk. Several worms from the 2009 study (filled symbols) augment numbers of larger individuals to illustrate gonad extent in full maturity.
Mentions: We examined trophosome, gonad extent and gamete formation (Table 1) with onset of reproductive maturity in smaller animals. In 19 of 43 females and in 16 of 51 males, no gametes were seen in the sections; not until over 4 mm diameter did a majority of the females have oocytes when gonad began to enlarge. Only four individuals were over 7.5 mm diameter in this sample set but comparison with R. piscesae from the 2009 collection shows at larger sizes (over 10 mm vestimentum diameter) there is a marked increase in gonad extent, most notable in males (Figure 4). Trophosome area increased variably with vestimentum size (Spearman r = 0.58, p<0.01) to a maximum of 50% of the body area; there was no significant correlation with gonad size.

Bottom Line: This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment.Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms.This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Victoria, Victoria, British Columbia, Canada; School of Earth & Ocean Sciences, University of Victoria, Victoria, British Columbia, Canada.

ABSTRACT
We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a "short-fat" phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

Show MeSH