Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)

Andrea Bernard; Rebekah L. Horn; Demian D. Chapman; Kevin A. Feldheim; Ricardo C. Garla; Edd J. Brooks; Mauvis A. Gore; Mahmood S. Shivji

doi:10.1111/jbi.13062

Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)

Andrea Bernard
, Rebekah L. Horn
, Demian D. Chapman
, Kevin A. Feldheim
, Ricardo C. Garla
, Edd J. Brooks
, Mauvis A. Gore
, Mahmood S. Shivji

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

Abstract

Aim

The Caribbean reef shark ( Carcharhinus perezi ) is one of few extant reef sharks inhabiting the Atlantic Ocean. Its variability in movements across habitat types suggests the possibility of a complex genetic population structure. Here, we use mitochondrial and nuclear DNA to investigate the genetic connectivity of the Caribbean reef shark across contemporary and evolutionary time-scales and relate our findings to the ecology of this understudied species.

Location

Tropical western Atlantic and Caribbean.

Methods

Samples were obtained from 216 individuals from six western Atlantic and Caribbean locations. Individuals were genotyped at seven nuclear microsatellite DNA loci and sequenced at two mitochondrial (control region [CR]; NADH dehydrogenase subunit 4 [ND4]) and one nuclear locus (lactate dehydrogenase [LDH]). Analyses to resolve the population genetic structure and evolutionary history of this species were adopted.

Results

Sequencing of the CR (1,068 bp, n = 216), ND4 (741 bp, n = 213) and LDH (258 bp, n = 165) loci, resolved 11, 8 and 13 unique haplotypes (or alleles), respectively. Overall, Caribbean reef sharks showed low levels of genetic diversity and most marker sets identified strong genetic differences ( F _ST and Φ _ST ) between sharks sampled in Brazil versus all other locations (msat F _ST > 0.017; CR-ND4 Φ _ST > 0.013). Mitochondrial DNA showed evidence of increased genetic partitioning among western North Atlantic sampling sites, although widespread haplotype sharing (~85%–92%) and a shallow population history were found.

Main Conclusions

Findings of genetic differentiation are concordant with previous movement studies showing residency and/or site-fidelity to specific locations by individuals. However, similar to other reef shark studies, we found that the level of genetic connectivity among populations was context dependent—i.e., sharks occupying isolated habitats showed greater genetic differentiation compared with those sharks occupying semi-isolated or continuous reef habitats. Furthermore, low genetic diversity and a shallow mitochondrial population history were found, suggesting historical demographic fluctuations, including population collapse and more recent expansions.

Original language	American English
Pages (from-to)	2488-2500
Number of pages	13
Journal	Journal of Biogeography
Volume	44
Issue number	11
DOIs	https://doi.org/10.1111/jbi.13062
State	Published - Jul 26 2017

Bibliographical note

Publisher Copyright:
© 2017 John Wiley & Sons Ltd

Funding

Funding was provided by Save Our Seas Foundation (MSS), Guy Harvey Ocean Foundation (MSS), Shark Foundation/Hai Stiftung (MSS), Cape Eleuthera Foundation (The Bahamas), Overseas Territories Environmental Programme (Cayman Islands), the Pritzker Foundation (microsatellite enrichment and development), Wildlife Conservation Society Marine Fellowship Program (to DDC and RG), São Paulo Research Foundation (FAPESP, Grant #1998/ 15080-8), the PADI Foundation (DDC), and Project AWARE (DDC). Support was provided by the Cayman Islands Department of Environment and the Pritzker Laboratory for Molecular Systematics and Evolution. All sampling and research was carried out under the authorization and guidelines of the following agencies: US Virgin Islands Department of Planning and Natural Resources, Division of Fish and Wildlife scientific collection permit # STT-011-07 (MSS); Belize Department of Fisheries Annual Research Permit (DDC); The Brazilian Environmental Agency (IBAMA, #02001, 000111/99-36) and the General Administration of the State District of Fernando de Noronha (RCG); The Bahamian Department of Marine Resources ((EJB) (Cape Eleuthera Institute Permit #MAF/FIS/17 and MAF/FIS/34); Cayman Islands’ Department of Environment (MAG). Save Our Seas Foundation; Guy Harvey Ocean Foundation; Shark Foundation/Hai Stiftung; Cape Eleuthera Foundation; Overseas Territories Environmental Programme; the Pritzker Foundation; Wildlife Conservation Society Marine Fellowship Program; São Paulo Research Foundation, Grant/Award Number: FAPESP, Grant #1998/15080-8; PADI Foundation; Project AWARE

Funders	Funder number
Overseas Territories Environmental Programme
Shark Foundation/Hai-Stiftung
PADI Foundation
Wildlife Conservation Society
Direktion für Entwicklung und Zusammenarbeit
Cape Eleuthera Foundation
Guy Harvey Ocean Foundation
Pritzker Pucker Family Foundation
Fundação de Amparo à Pesquisa do Estado de São Paulo	1998/ 15080-8
Save our Seas Foundation
Ministry of SMEs and Startups

ASJC Scopus Subject Areas

Ecology, Evolution, Behavior and Systematics
Ecology

Keywords

Coral reefs
Elasmobranch
Evolutionary history
Marine biogeography
Microsatellite DNA
Mitochondrial DNA
Population structure
Western Atlantic
population structure
mitochondrial DNA
western Atlantic
coral reefs
marine biogeography
elasmobranch
evolutionary history
microsatellite DNA

Disciplines

Marine Biology
Oceanography and Atmospheric Sciences and Meteorology

Access to Document

10.1111/jbi.13062

Cite this

@article{6fe99c832f5149a7bf36b12e3a66b86d,

title = "Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)",

abstract = " Aim The Caribbean reef shark ( Carcharhinus perezi ) is one of few extant reef sharks inhabiting the Atlantic Ocean. Its variability in movements across habitat types suggests the possibility of a complex genetic population structure. Here, we use mitochondrial and nuclear DNA to investigate the genetic connectivity of the Caribbean reef shark across contemporary and evolutionary time-scales and relate our findings to the ecology of this understudied species. Location Tropical western Atlantic and Caribbean. Methods Samples were obtained from 216 individuals from six western Atlantic and Caribbean locations. Individuals were genotyped at seven nuclear microsatellite DNA loci and sequenced at two mitochondrial (control region [CR]; NADH dehydrogenase subunit 4 [ND4]) and one nuclear locus (lactate dehydrogenase [LDH]). Analyses to resolve the population genetic structure and evolutionary history of this species were adopted. Results Sequencing of the CR (1,068 bp, n = 216), ND4 (741 bp, n = 213) and LDH (258 bp, n = 165) loci, resolved 11, 8 and 13 unique haplotypes (or alleles), respectively. Overall, Caribbean reef sharks showed low levels of genetic diversity and most marker sets identified strong genetic differences ( F ST and Φ ST ) between sharks sampled in Brazil versus all other locations (msat F ST > 0.017; CR-ND4 Φ ST > 0.013). Mitochondrial DNA showed evidence of increased genetic partitioning among western North Atlantic sampling sites, although widespread haplotype sharing (\textasciitilde{}85\%–92\%) and a shallow population history were found. Main Conclusions Findings of genetic differentiation are concordant with previous movement studies showing residency and/or site-fidelity to specific locations by individuals. However, similar to other reef shark studies, we found that the level of genetic connectivity among populations was context dependent—i.e., sharks occupying isolated habitats showed greater genetic differentiation compared with those sharks occupying semi-isolated or continuous reef habitats. Furthermore, low genetic diversity and a shallow mitochondrial population history were found, suggesting historical demographic fluctuations, including population collapse and more recent expansions.",

keywords = "Coral reefs, Elasmobranch, Evolutionary history, Marine biogeography, Microsatellite DNA, Mitochondrial DNA, Population structure, Western Atlantic, population structure, mitochondrial DNA, western Atlantic, coral reefs, marine biogeography, elasmobranch, evolutionary history, microsatellite DNA",

author = "Andrea Bernard and Horn, \{Rebekah L.\} and Chapman, \{Demian D.\} and Feldheim, \{Kevin A.\} and Garla, \{Ricardo C.\} and Brooks, \{Edd J.\} and Gore, \{Mauvis A.\} and Shivji, \{Mahmood S.\}",

note = "Publisher Copyright: {\textcopyright} 2017 John Wiley \& Sons Ltd",

year = "2017",

month = jul,

day = "26",

doi = "10.1111/jbi.13062",

language = "American English",

volume = "44",

pages = "2488--2500",

journal = "Journal of Biogeography",

issn = "0305-0270",

number = "11",

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TY - JOUR

T1 - Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)

AU - Bernard, Andrea

AU - Horn, Rebekah L.

AU - Chapman, Demian D.

AU - Feldheim, Kevin A.

AU - Garla, Ricardo C.

AU - Brooks, Edd J.

AU - Gore, Mauvis A.

AU - Shivji, Mahmood S.

PY - 2017/7/26

Y1 - 2017/7/26

N2 - Aim The Caribbean reef shark ( Carcharhinus perezi ) is one of few extant reef sharks inhabiting the Atlantic Ocean. Its variability in movements across habitat types suggests the possibility of a complex genetic population structure. Here, we use mitochondrial and nuclear DNA to investigate the genetic connectivity of the Caribbean reef shark across contemporary and evolutionary time-scales and relate our findings to the ecology of this understudied species. Location Tropical western Atlantic and Caribbean. Methods Samples were obtained from 216 individuals from six western Atlantic and Caribbean locations. Individuals were genotyped at seven nuclear microsatellite DNA loci and sequenced at two mitochondrial (control region [CR]; NADH dehydrogenase subunit 4 [ND4]) and one nuclear locus (lactate dehydrogenase [LDH]). Analyses to resolve the population genetic structure and evolutionary history of this species were adopted. Results Sequencing of the CR (1,068 bp, n = 216), ND4 (741 bp, n = 213) and LDH (258 bp, n = 165) loci, resolved 11, 8 and 13 unique haplotypes (or alleles), respectively. Overall, Caribbean reef sharks showed low levels of genetic diversity and most marker sets identified strong genetic differences ( F ST and Φ ST ) between sharks sampled in Brazil versus all other locations (msat F ST > 0.017; CR-ND4 Φ ST > 0.013). Mitochondrial DNA showed evidence of increased genetic partitioning among western North Atlantic sampling sites, although widespread haplotype sharing (~85%–92%) and a shallow population history were found. Main Conclusions Findings of genetic differentiation are concordant with previous movement studies showing residency and/or site-fidelity to specific locations by individuals. However, similar to other reef shark studies, we found that the level of genetic connectivity among populations was context dependent—i.e., sharks occupying isolated habitats showed greater genetic differentiation compared with those sharks occupying semi-isolated or continuous reef habitats. Furthermore, low genetic diversity and a shallow mitochondrial population history were found, suggesting historical demographic fluctuations, including population collapse and more recent expansions.

AB - Aim The Caribbean reef shark ( Carcharhinus perezi ) is one of few extant reef sharks inhabiting the Atlantic Ocean. Its variability in movements across habitat types suggests the possibility of a complex genetic population structure. Here, we use mitochondrial and nuclear DNA to investigate the genetic connectivity of the Caribbean reef shark across contemporary and evolutionary time-scales and relate our findings to the ecology of this understudied species. Location Tropical western Atlantic and Caribbean. Methods Samples were obtained from 216 individuals from six western Atlantic and Caribbean locations. Individuals were genotyped at seven nuclear microsatellite DNA loci and sequenced at two mitochondrial (control region [CR]; NADH dehydrogenase subunit 4 [ND4]) and one nuclear locus (lactate dehydrogenase [LDH]). Analyses to resolve the population genetic structure and evolutionary history of this species were adopted. Results Sequencing of the CR (1,068 bp, n = 216), ND4 (741 bp, n = 213) and LDH (258 bp, n = 165) loci, resolved 11, 8 and 13 unique haplotypes (or alleles), respectively. Overall, Caribbean reef sharks showed low levels of genetic diversity and most marker sets identified strong genetic differences ( F ST and Φ ST ) between sharks sampled in Brazil versus all other locations (msat F ST > 0.017; CR-ND4 Φ ST > 0.013). Mitochondrial DNA showed evidence of increased genetic partitioning among western North Atlantic sampling sites, although widespread haplotype sharing (~85%–92%) and a shallow population history were found. Main Conclusions Findings of genetic differentiation are concordant with previous movement studies showing residency and/or site-fidelity to specific locations by individuals. However, similar to other reef shark studies, we found that the level of genetic connectivity among populations was context dependent—i.e., sharks occupying isolated habitats showed greater genetic differentiation compared with those sharks occupying semi-isolated or continuous reef habitats. Furthermore, low genetic diversity and a shallow mitochondrial population history were found, suggesting historical demographic fluctuations, including population collapse and more recent expansions.

KW - Coral reefs

KW - Elasmobranch

KW - Evolutionary history

KW - Marine biogeography

KW - Microsatellite DNA

KW - Mitochondrial DNA

KW - Population structure

KW - Western Atlantic

KW - population structure

KW - mitochondrial DNA

KW - western Atlantic

KW - coral reefs

KW - marine biogeography

KW - elasmobranch

KW - evolutionary history

KW - microsatellite DNA

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U2 - 10.1111/jbi.13062

DO - 10.1111/jbi.13062

M3 - Article

SN - 0305-0270

VL - 44

SP - 2488

EP - 2500

JO - Journal of Biogeography

JF - Journal of Biogeography

IS - 11

ER -

Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)

Abstract

Bibliographical note

Funding

ASJC Scopus Subject Areas

Keywords

Disciplines

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