Spatial and environmental variables structure sponge symbiont communities

D F R Cleary; Ana R. M. Polónia; Thomas Swierts; Francisco J. R. C. Coelho; Nicole J. de Voogd; Newton C. M. Gomes

doi:10.1111/mec.16631

Spatial and environmental variables structure sponge symbiont communities

D F R Cleary, Ana R. M. Polónia, Thomas Swierts, Francisco J. R. C. Coelho, Nicole J. de Voogd, Newton C. M. Gomes

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes remain unclear, particularly for host-prokaryotic associations. Here, beta diversity patterns were studied in five prokaryotic biotopes, namely, two high microbial abundance (HMA) sponge taxa (Xestospongia spp. and Hyrtios erectus), one low microbial abundance (LMA) sponge taxon (Stylissa carteri), sediment and seawater sampled across thousands of kilometers. Using multiple regression on distance matrices (MRM), spatial (geographic distance) and environmental (sea surface temperature and chlorophyll a concentrations) variables proved significant predictors of beta diversity in all five biotopes and together explained from 54% to 82% of variation in dissimilarity of both HMA species, 27% to 43% of variation in sediment and seawater, but only 20% of variation of the LMA S. carteri. Variance partitioning was subsequently used to partition the variation into purely spatial, purely environmental and spatially-structured environmental components. The amount of variation in dissimilarity explained by the purely spatial component was lowest for S. carteri at 11% and highest for H. erectus at 55%. The purely environmental component, in turn, only explained from 0.15 to 2.83% of variation in all biotopes. In addition to spatial and environmental variables, a matrix of genetic differences between pairs of sponge individuals also proved a significant predictor of variation in prokaryotic composition of the Xestospongia species complex. We discuss the implications of these results for the HMA-LMA dichotomy and compare the MRM results with results obtained using constrained ordination and zeta diversity.

Original language	English (US)
Journal	Molecular Ecology
DOIs	https://doi.org/10.1111/mec.16631
State	Published - Jul 26 2022
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2022-09-14
Acknowledgements: This work was supported by European Funds through COMPETE [FCOMP-01-0124-FEDER-008657] and by National Funds through the Portuguese Foundation for Science and Technology (FCT) within the LESS CORAL [PTDC/AAC-AMB/115304/2009] and Ecotech-Sponge (PTDC/BIAMIC/6473/2014 – POCI-01-0145-FEDER-016531) projects. This work is also part of the research programme NWO-VIDI with project number 16.161.301, which was (partly) financed by the Netherlands Organisation for Scientific Research (NWO). We acknowledge financial support to CESAM from FCT/MCTES (UIDP/50017/2020+ UIDB/50017/2020 + LA/P/0094/2020), through national funds. FJRCC was funded by national funds through FC T under the Scientific Employment Sti mulus - Individual Call - reference CEECIND/00070/2017. Ana R.M. Polónia (postdoctoral scholarship: SFRH/BPD/117563/2016) was supported by a scholarship funded by FCT, Portugal within the Human Capital Operational Programme (HCOP), subsidised by the European Social Fund (ESF) and national funds (MCTES). We are also grateful to: 1) King Abdullah University of Science and Technology - Kingdom of Saudi Arabia (2399 KAUST-Naturalis; Red Sea); 2) Ministry of Fisheries and Agriculture of Maldives (OTHR) (Research permit # 30-D/INDIV/2015/56); 3) Ministry of Science and Technology (MOST) and Marine National Parks Headquarter of Taiwan (MNPH; MOST 105-2621-B-346-002 and MNPH 10443; Research permit: # 20160316364); 4) Universitas Sam Ratulangi (UNSRAT in Manado) and the Bitung field station of the Research Centre of Oceanography (PPO-LIPI) and its former director Prof. Dr. Suharsono (Lembeh); 5) Terres Australes en Antartiques françaises (TAAF) (Mayotte); 6) National Research Council of Thailand (NRCT) (Research permit # 0002/2032); 7) Department of Marine Biodiversity and Conservation, Research Institute for Marine Fisheries in Vietnam; 8) Lim Swee Cheng (Singapore); 9) Indonesian State Ministry for Research and Technology (Kementerian Riset Dan Teknologi Republik Indonesia – RISTEK Research permit # 283/SIP/FRP/SM/V/2021; Spermonde Archipelago). We thank Friso Dekker, Maarten van Gemert, Christine Hörnlein, Lisa Becking, Yusheng Huang, Laurie van Reemst, Ee Crovetto, Rossana Freitas, Anne Bialecki, Mike Berumen, Jaaziel Garcia Hernandez, Sumaitt Putchakarn, Chad Scott, Nguyen Khac Bat, Swee Cheng Lim, Zarinah Waheed, Yosephine Tuti, Betsie Voetdijk, Peter Kuperus and Marcel Eurlings for logistical support, field and laboratory assistance.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics

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10.1111/mec.16631

Cite this

@article{aa70a3d4102e492bac4364289fe3aac3,

title = "Spatial and environmental variables structure sponge symbiont communities",

abstract = "Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes remain unclear, particularly for host-prokaryotic associations. Here, beta diversity patterns were studied in five prokaryotic biotopes, namely, two high microbial abundance (HMA) sponge taxa (Xestospongia spp. and Hyrtios erectus), one low microbial abundance (LMA) sponge taxon (Stylissa carteri), sediment and seawater sampled across thousands of kilometers. Using multiple regression on distance matrices (MRM), spatial (geographic distance) and environmental (sea surface temperature and chlorophyll a concentrations) variables proved significant predictors of beta diversity in all five biotopes and together explained from 54% to 82% of variation in dissimilarity of both HMA species, 27% to 43% of variation in sediment and seawater, but only 20% of variation of the LMA S. carteri. Variance partitioning was subsequently used to partition the variation into purely spatial, purely environmental and spatially-structured environmental components. The amount of variation in dissimilarity explained by the purely spatial component was lowest for S. carteri at 11% and highest for H. erectus at 55%. The purely environmental component, in turn, only explained from 0.15 to 2.83% of variation in all biotopes. In addition to spatial and environmental variables, a matrix of genetic differences between pairs of sponge individuals also proved a significant predictor of variation in prokaryotic composition of the Xestospongia species complex. We discuss the implications of these results for the HMA-LMA dichotomy and compare the MRM results with results obtained using constrained ordination and zeta diversity.",

author = "Cleary, {D F R} and Pol{\'o}nia, {Ana R. M.} and Thomas Swierts and Coelho, {Francisco J. R. C.} and {de Voogd}, {Nicole J.} and Gomes, {Newton C. M.}",

note = "KAUST Repository Item: Exported on 2022-09-14 Acknowledgements: This work was supported by European Funds through COMPETE [FCOMP-01-0124-FEDER-008657] and by National Funds through the Portuguese Foundation for Science and Technology (FCT) within the LESS CORAL [PTDC/AAC-AMB/115304/2009] and Ecotech-Sponge (PTDC/BIAMIC/6473/2014 – POCI-01-0145-FEDER-016531) projects. This work is also part of the research programme NWO-VIDI with project number 16.161.301, which was (partly) financed by the Netherlands Organisation for Scientific Research (NWO). We acknowledge financial support to CESAM from FCT/MCTES (UIDP/50017/2020+ UIDB/50017/2020 + LA/P/0094/2020), through national funds. FJRCC was funded by national funds through FC T under the Scientific Employment Sti mulus - Individual Call - reference CEECIND/00070/2017. Ana R.M. Pol{\'o}nia (postdoctoral scholarship: SFRH/BPD/117563/2016) was supported by a scholarship funded by FCT, Portugal within the Human Capital Operational Programme (HCOP), subsidised by the European Social Fund (ESF) and national funds (MCTES). We are also grateful to: 1) King Abdullah University of Science and Technology - Kingdom of Saudi Arabia (2399 KAUST-Naturalis; Red Sea); 2) Ministry of Fisheries and Agriculture of Maldives (OTHR) (Research permit # 30-D/INDIV/2015/56); 3) Ministry of Science and Technology (MOST) and Marine National Parks Headquarter of Taiwan (MNPH; MOST 105-2621-B-346-002 and MNPH 10443; Research permit: # 20160316364); 4) Universitas Sam Ratulangi (UNSRAT in Manado) and the Bitung field station of the Research Centre of Oceanography (PPO-LIPI) and its former director Prof. Dr. Suharsono (Lembeh); 5) Terres Australes en Antartiques fran{\c c}aises (TAAF) (Mayotte); 6) National Research Council of Thailand (NRCT) (Research permit # 0002/2032); 7) Department of Marine Biodiversity and Conservation, Research Institute for Marine Fisheries in Vietnam; 8) Lim Swee Cheng (Singapore); 9) Indonesian State Ministry for Research and Technology (Kementerian Riset Dan Teknologi Republik Indonesia – RISTEK Research permit # 283/SIP/FRP/SM/V/2021; Spermonde Archipelago). We thank Friso Dekker, Maarten van Gemert, Christine H{\"o}rnlein, Lisa Becking, Yusheng Huang, Laurie van Reemst, Ee Crovetto, Rossana Freitas, Anne Bialecki, Mike Berumen, Jaaziel Garcia Hernandez, Sumaitt Putchakarn, Chad Scott, Nguyen Khac Bat, Swee Cheng Lim, Zarinah Waheed, Yosephine Tuti, Betsie Voetdijk, Peter Kuperus and Marcel Eurlings for logistical support, field and laboratory assistance. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

year = "2022",

month = jul,

day = "26",

doi = "10.1111/mec.16631",

language = "English (US)",

journal = "Molecular Ecology",

issn = "0962-1083",

publisher = "Wiley",

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TY - JOUR

T1 - Spatial and environmental variables structure sponge symbiont communities

AU - Cleary, D F R

AU - Polónia, Ana R. M.

AU - Swierts, Thomas

AU - Coelho, Francisco J. R. C.

AU - de Voogd, Nicole J.

AU - Gomes, Newton C. M.

N1 - KAUST Repository Item: Exported on 2022-09-14 Acknowledgements: This work was supported by European Funds through COMPETE [FCOMP-01-0124-FEDER-008657] and by National Funds through the Portuguese Foundation for Science and Technology (FCT) within the LESS CORAL [PTDC/AAC-AMB/115304/2009] and Ecotech-Sponge (PTDC/BIAMIC/6473/2014 – POCI-01-0145-FEDER-016531) projects. This work is also part of the research programme NWO-VIDI with project number 16.161.301, which was (partly) financed by the Netherlands Organisation for Scientific Research (NWO). We acknowledge financial support to CESAM from FCT/MCTES (UIDP/50017/2020+ UIDB/50017/2020 + LA/P/0094/2020), through national funds. FJRCC was funded by national funds through FC T under the Scientific Employment Sti mulus - Individual Call - reference CEECIND/00070/2017. Ana R.M. Polónia (postdoctoral scholarship: SFRH/BPD/117563/2016) was supported by a scholarship funded by FCT, Portugal within the Human Capital Operational Programme (HCOP), subsidised by the European Social Fund (ESF) and national funds (MCTES). We are also grateful to: 1) King Abdullah University of Science and Technology - Kingdom of Saudi Arabia (2399 KAUST-Naturalis; Red Sea); 2) Ministry of Fisheries and Agriculture of Maldives (OTHR) (Research permit # 30-D/INDIV/2015/56); 3) Ministry of Science and Technology (MOST) and Marine National Parks Headquarter of Taiwan (MNPH; MOST 105-2621-B-346-002 and MNPH 10443; Research permit: # 20160316364); 4) Universitas Sam Ratulangi (UNSRAT in Manado) and the Bitung field station of the Research Centre of Oceanography (PPO-LIPI) and its former director Prof. Dr. Suharsono (Lembeh); 5) Terres Australes en Antartiques françaises (TAAF) (Mayotte); 6) National Research Council of Thailand (NRCT) (Research permit # 0002/2032); 7) Department of Marine Biodiversity and Conservation, Research Institute for Marine Fisheries in Vietnam; 8) Lim Swee Cheng (Singapore); 9) Indonesian State Ministry for Research and Technology (Kementerian Riset Dan Teknologi Republik Indonesia – RISTEK Research permit # 283/SIP/FRP/SM/V/2021; Spermonde Archipelago). We thank Friso Dekker, Maarten van Gemert, Christine Hörnlein, Lisa Becking, Yusheng Huang, Laurie van Reemst, Ee Crovetto, Rossana Freitas, Anne Bialecki, Mike Berumen, Jaaziel Garcia Hernandez, Sumaitt Putchakarn, Chad Scott, Nguyen Khac Bat, Swee Cheng Lim, Zarinah Waheed, Yosephine Tuti, Betsie Voetdijk, Peter Kuperus and Marcel Eurlings for logistical support, field and laboratory assistance. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2022/7/26

Y1 - 2022/7/26

N2 - Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes remain unclear, particularly for host-prokaryotic associations. Here, beta diversity patterns were studied in five prokaryotic biotopes, namely, two high microbial abundance (HMA) sponge taxa (Xestospongia spp. and Hyrtios erectus), one low microbial abundance (LMA) sponge taxon (Stylissa carteri), sediment and seawater sampled across thousands of kilometers. Using multiple regression on distance matrices (MRM), spatial (geographic distance) and environmental (sea surface temperature and chlorophyll a concentrations) variables proved significant predictors of beta diversity in all five biotopes and together explained from 54% to 82% of variation in dissimilarity of both HMA species, 27% to 43% of variation in sediment and seawater, but only 20% of variation of the LMA S. carteri. Variance partitioning was subsequently used to partition the variation into purely spatial, purely environmental and spatially-structured environmental components. The amount of variation in dissimilarity explained by the purely spatial component was lowest for S. carteri at 11% and highest for H. erectus at 55%. The purely environmental component, in turn, only explained from 0.15 to 2.83% of variation in all biotopes. In addition to spatial and environmental variables, a matrix of genetic differences between pairs of sponge individuals also proved a significant predictor of variation in prokaryotic composition of the Xestospongia species complex. We discuss the implications of these results for the HMA-LMA dichotomy and compare the MRM results with results obtained using constrained ordination and zeta diversity.

AB - Understanding the maintenance and origin of beta diversity is a central topic in ecology. However, the factors that drive diversity patterns and underlying processes remain unclear, particularly for host-prokaryotic associations. Here, beta diversity patterns were studied in five prokaryotic biotopes, namely, two high microbial abundance (HMA) sponge taxa (Xestospongia spp. and Hyrtios erectus), one low microbial abundance (LMA) sponge taxon (Stylissa carteri), sediment and seawater sampled across thousands of kilometers. Using multiple regression on distance matrices (MRM), spatial (geographic distance) and environmental (sea surface temperature and chlorophyll a concentrations) variables proved significant predictors of beta diversity in all five biotopes and together explained from 54% to 82% of variation in dissimilarity of both HMA species, 27% to 43% of variation in sediment and seawater, but only 20% of variation of the LMA S. carteri. Variance partitioning was subsequently used to partition the variation into purely spatial, purely environmental and spatially-structured environmental components. The amount of variation in dissimilarity explained by the purely spatial component was lowest for S. carteri at 11% and highest for H. erectus at 55%. The purely environmental component, in turn, only explained from 0.15 to 2.83% of variation in all biotopes. In addition to spatial and environmental variables, a matrix of genetic differences between pairs of sponge individuals also proved a significant predictor of variation in prokaryotic composition of the Xestospongia species complex. We discuss the implications of these results for the HMA-LMA dichotomy and compare the MRM results with results obtained using constrained ordination and zeta diversity.

UR - http://hdl.handle.net/10754/679977

UR - https://onlinelibrary.wiley.com/doi/10.1111/mec.16631

U2 - 10.1111/mec.16631

DO - 10.1111/mec.16631

M3 - Article

C2 - 35881675

SN - 0962-1083

JO - Molecular Ecology

JF - Molecular Ecology

ER -

Spatial and environmental variables structure sponge symbiont communities

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