Biophysical and Population Genetic Models Predict the Presence of “Phantom” Stepping Stones Connecting Mid-Atlantic Ridge Vent Ecosystems

Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns...

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Published inCurrent biology Vol. 26; no. 17; pp. 2257 - 2267
Main Authors Breusing, Corinna, Biastoch, Arne, Drews, Annika, Metaxas, Anna, Jollivet, Didier, Vrijenhoek, Robert C., Bayer, Till, Melzner, Frank, Sayavedra, Lizbeth, Petersen, Jillian M., Dubilier, Nicole, Schilhabel, Markus B., Rosenstiel, Philip, Reusch, Thorsten B.H.
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 12.09.2016
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Online AccessGet full text
ISSN0960-9822
1879-0445
1879-0445
DOI10.1016/j.cub.2016.06.062

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Abstract Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats (“phantom” stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas. •Mid-Atlantic vent mussel populations are contemporarily isolated•Population connectivity can only be maintained in a stepwise manner•Four mussel lineages exist on the Mid-Atlantic Ridge•Recolonization of perturbed vent localities is uncertain Assessment of contemporary connectivity in hydrothermal vents is critical for a thorough understanding of vent biology and the mitigation of environmental impacts from deep-sea mining. In contrast to previous assumptions, Breusing et al. show that connections between mid-Atlantic vent mussel populations can only be achieved via stepping-stone habitats.
AbstractList Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats ("phantom" stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas.Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats ("phantom" stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas.
Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats (“phantom” stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas. •Mid-Atlantic vent mussel populations are contemporarily isolated•Population connectivity can only be maintained in a stepwise manner•Four mussel lineages exist on the Mid-Atlantic Ridge•Recolonization of perturbed vent localities is uncertain Assessment of contemporary connectivity in hydrothermal vents is critical for a thorough understanding of vent biology and the mitigation of environmental impacts from deep-sea mining. In contrast to previous assumptions, Breusing et al. show that connections between mid-Atlantic vent mussel populations can only be achieved via stepping-stone habitats.
Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats ("phantom" stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas.
Author Reusch, Thorsten B.H.
Schilhabel, Markus B.
Metaxas, Anna
Drews, Annika
Biastoch, Arne
Melzner, Frank
Petersen, Jillian M.
Jollivet, Didier
Bayer, Till
Vrijenhoek, Robert C.
Rosenstiel, Philip
Sayavedra, Lizbeth
Dubilier, Nicole
Breusing, Corinna
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  fullname: Jollivet, Didier
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  fullname: Melzner, Frank
  organization: GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany
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  givenname: Lizbeth
  surname: Sayavedra
  fullname: Sayavedra, Lizbeth
  organization: Symbiosis Department, Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany
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  givenname: Jillian M.
  surname: Petersen
  fullname: Petersen, Jillian M.
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  fullname: Dubilier, Nicole
  organization: Symbiosis Department, Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany
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  givenname: Markus B.
  surname: Schilhabel
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  surname: Reusch
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Snippet Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many...
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SubjectTerms Animal Distribution
Animals
Atlantic Ocean
Ecosystem
Genetic Variation
Hydrothermal Vents
Larva - genetics
Larva - growth & development
Models, Genetic
Models, Theoretical
Mytilidae - genetics
Mytilidae - growth & development
Mytilidae - physiology
Sequence Analysis, DNA
Title Biophysical and Population Genetic Models Predict the Presence of “Phantom” Stepping Stones Connecting Mid-Atlantic Ridge Vent Ecosystems
URI https://dx.doi.org/10.1016/j.cub.2016.06.062
https://www.ncbi.nlm.nih.gov/pubmed/27476600
https://www.proquest.com/docview/1819902464
Volume 26
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