Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

Aaron C. Hartmann, Kristen L. Marhaver, Anke Klueter, Michael T. Lovci, Collin J. Closek, Erika Diaz, Valérie F. Chamberland, Frederick I. Archer, Dimitri D. Deheyn, Mark J.A. Vermeij, Mónica Medina

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

Original languageEnglish (US)
Pages (from-to)141-155
Number of pages15
JournalMolecular ecology
Volume28
Issue number1
DOIs
StatePublished - Jan 2019

Fingerprint

Anthozoa
symbiont
symbionts
Larva
corals
coral
Marine Biology
Genetic Fitness
endosymbiont
Coral Reefs
endosymbionts
Dinoflagellida
larva
Symbiosis
larvae
reefs
reef
energetics
Eggs
vertical transmission

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Hartmann, A. C., Marhaver, K. L., Klueter, A., Lovci, M. T., Closek, C. J., Diaz, E., ... Medina, M. (2019). Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host. Molecular ecology, 28(1), 141-155. https://doi.org/10.1111/mec.14967
Hartmann, Aaron C. ; Marhaver, Kristen L. ; Klueter, Anke ; Lovci, Michael T. ; Closek, Collin J. ; Diaz, Erika ; Chamberland, Valérie F. ; Archer, Frederick I. ; Deheyn, Dimitri D. ; Vermeij, Mark J.A. ; Medina, Mónica. / Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host. In: Molecular ecology. 2019 ; Vol. 28, No. 1. pp. 141-155.
@article{b5c86613c6564c8ca2b63355dda2c174,
title = "Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host",
abstract = "Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.",
author = "Hartmann, {Aaron C.} and Marhaver, {Kristen L.} and Anke Klueter and Lovci, {Michael T.} and Closek, {Collin J.} and Erika Diaz and Chamberland, {Val{\'e}rie F.} and Archer, {Frederick I.} and Deheyn, {Dimitri D.} and Vermeij, {Mark J.A.} and M{\'o}nica Medina",
year = "2019",
month = "1",
doi = "10.1111/mec.14967",
language = "English (US)",
volume = "28",
pages = "141--155",
journal = "Molecular Ecology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "1",

}

Hartmann, AC, Marhaver, KL, Klueter, A, Lovci, MT, Closek, CJ, Diaz, E, Chamberland, VF, Archer, FI, Deheyn, DD, Vermeij, MJA & Medina, M 2019, 'Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host', Molecular ecology, vol. 28, no. 1, pp. 141-155. https://doi.org/10.1111/mec.14967

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host. / Hartmann, Aaron C.; Marhaver, Kristen L.; Klueter, Anke; Lovci, Michael T.; Closek, Collin J.; Diaz, Erika; Chamberland, Valérie F.; Archer, Frederick I.; Deheyn, Dimitri D.; Vermeij, Mark J.A.; Medina, Mónica.

In: Molecular ecology, Vol. 28, No. 1, 01.2019, p. 141-155.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

AU - Hartmann, Aaron C.

AU - Marhaver, Kristen L.

AU - Klueter, Anke

AU - Lovci, Michael T.

AU - Closek, Collin J.

AU - Diaz, Erika

AU - Chamberland, Valérie F.

AU - Archer, Frederick I.

AU - Deheyn, Dimitri D.

AU - Vermeij, Mark J.A.

AU - Medina, Mónica

PY - 2019/1

Y1 - 2019/1

N2 - Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

AB - Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

UR - http://www.scopus.com/inward/record.url?scp=85060369259&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060369259&partnerID=8YFLogxK

U2 - 10.1111/mec.14967

DO - 10.1111/mec.14967

M3 - Article

C2 - 30506836

AN - SCOPUS:85060369259

VL - 28

SP - 141

EP - 155

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 1

ER -