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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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Female reproductive condition in Ridgeia piscesae in high, moderate and low flux habitats.Indicators reflect that females from the high flux samples have greater reproductive output; bars are sd. A. Total lipid content in trunks of 12 individuals.B. Gonad volume estimated from trunk sections. C. Total oocytes estimated from section counts and gonad volume. Neither moderate nor low flux worms had oocytes in ovisacs ready for release.
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pone-0110578-g007: Female reproductive condition in Ridgeia piscesae in high, moderate and low flux habitats.Indicators reflect that females from the high flux samples have greater reproductive output; bars are sd. A. Total lipid content in trunks of 12 individuals.B. Gonad volume estimated from trunk sections. C. Total oocytes estimated from section counts and gonad volume. Neither moderate nor low flux worms had oocytes in ovisacs ready for release.

Mentions: The largest lipid values occurred in females from a high temperature setting (26°C) (Figure 7A). Overall gonad volume was much larger in high flux individuals than moderate (10°C) or low (4°C) flux (Mann-Whitney, p<0.01) and oocytes in the oviducts more abundant in high flux (Figure 7B, C). The overall estimate of fecundity was 56,000 oocytes in high flux versus 27,000 in moderate or low when oocytes were present; however, only high flux worms had oocytes in the ovisacs ready for release. There were no significant differences among oocyte sizes from the three sites. Similarly, in males, the high flux animals displayed much greater amounts of gonad and trophosome as illustrated in the trunk cross-sections in Figure S1.


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)

Female reproductive condition in Ridgeia piscesae in high, moderate and low flux habitats.Indicators reflect that females from the high flux samples have greater reproductive output; bars are sd. A. Total lipid content in trunks of 12 individuals.B. Gonad volume estimated from trunk sections. C. Total oocytes estimated from section counts and gonad volume. Neither moderate nor low flux worms had oocytes in ovisacs ready for release.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0110578-g007: Female reproductive condition in Ridgeia piscesae in high, moderate and low flux habitats.Indicators reflect that females from the high flux samples have greater reproductive output; bars are sd. A. Total lipid content in trunks of 12 individuals.B. Gonad volume estimated from trunk sections. C. Total oocytes estimated from section counts and gonad volume. Neither moderate nor low flux worms had oocytes in ovisacs ready for release.
Mentions: The largest lipid values occurred in females from a high temperature setting (26°C) (Figure 7A). Overall gonad volume was much larger in high flux individuals than moderate (10°C) or low (4°C) flux (Mann-Whitney, p<0.01) and oocytes in the oviducts more abundant in high flux (Figure 7B, C). The overall estimate of fecundity was 56,000 oocytes in high flux versus 27,000 in moderate or low when oocytes were present; however, only high flux worms had oocytes in the ovisacs ready for release. There were no significant differences among oocyte sizes from the three sites. Similarly, in males, the high flux animals displayed much greater amounts of gonad and trophosome as illustrated in the trunk cross-sections in Figure S1.

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