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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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Model of reproductive readiness based on tube diameter.Onset of reproduction with size follows a logistic curve. The likelihood that an individual is reproductive at a given tube diameter is shown in the dotted line (left axis) using all individuals in our 2008 study. Tube diameter is highly correlated body characters but is an easier trait to measure. The right axis represents the proportion of the Endeavour samples that were reproductive (dots) and the full logistic curve (solid line) is the best fit for any sample taken.
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pone-0110578-g008: Model of reproductive readiness based on tube diameter.Onset of reproduction with size follows a logistic curve. The likelihood that an individual is reproductive at a given tube diameter is shown in the dotted line (left axis) using all individuals in our 2008 study. Tube diameter is highly correlated body characters but is an easier trait to measure. The right axis represents the proportion of the Endeavour samples that were reproductive (dots) and the full logistic curve (solid line) is the best fit for any sample taken.

Mentions: Of the 379 worms assessed for developmental state in the paired samples, 171 were considered non-reproducing with empty ovisacs or seminal vesicles; all these animals, except two, were under 6.7 mm tube diameter. All other tubeworms over 6 mm diameter were reproductive with abundant gametes. Figure 8 illustrates that an individual is likely to become reproductive between 5 and 6.5 mm diameter based on a logistic model that fits the observations well (Hosmer-Lemeshow test of goodness of fit, p<0.01). The model combines all individuals, however, the likelihood of individuals being reproductive between the size of 5 and 6.5 mm was significantly lower in low flux samples (Chi-Sq; p<0.01). The proportion of reproductive individuals within a sample follows the logistic curve, p = 1/(1+EXP(−1*(−11.3+2.1*ATD))) where ATD is anterior tube diameter (Figure 8).


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)

Model of reproductive readiness based on tube diameter.Onset of reproduction with size follows a logistic curve. The likelihood that an individual is reproductive at a given tube diameter is shown in the dotted line (left axis) using all individuals in our 2008 study. Tube diameter is highly correlated body characters but is an easier trait to measure. The right axis represents the proportion of the Endeavour samples that were reproductive (dots) and the full logistic curve (solid line) is the best fit for any sample taken.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0110578-g008: Model of reproductive readiness based on tube diameter.Onset of reproduction with size follows a logistic curve. The likelihood that an individual is reproductive at a given tube diameter is shown in the dotted line (left axis) using all individuals in our 2008 study. Tube diameter is highly correlated body characters but is an easier trait to measure. The right axis represents the proportion of the Endeavour samples that were reproductive (dots) and the full logistic curve (solid line) is the best fit for any sample taken.
Mentions: Of the 379 worms assessed for developmental state in the paired samples, 171 were considered non-reproducing with empty ovisacs or seminal vesicles; all these animals, except two, were under 6.7 mm tube diameter. All other tubeworms over 6 mm diameter were reproductive with abundant gametes. Figure 8 illustrates that an individual is likely to become reproductive between 5 and 6.5 mm diameter based on a logistic model that fits the observations well (Hosmer-Lemeshow test of goodness of fit, p<0.01). The model combines all individuals, however, the likelihood of individuals being reproductive between the size of 5 and 6.5 mm was significantly lower in low flux samples (Chi-Sq; p<0.01). The proportion of reproductive individuals within a sample follows the logistic curve, p = 1/(1+EXP(−1*(−11.3+2.1*ATD))) where ATD is anterior tube diameter (Figure 8).

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