Journal of Biogeography
SUPPORTING INFORMATION
Article title
Seascape features, rather than dispersal traits, predict spatial genetic patterns in codistributed reef fishes
Author names
Libby Liggins, Eric A. Treml, Hugh P. Possingham, and Cynthia Riginos
Appendix S1 Sampled locations for each species and related genetic diversity and
demographic statistics; Comparative analyses of genetic diversity patterns.
Appendix S2 Biological parameters for each species used in biophysical models of
‘dispersal distance’; Making a predictor matrix for the Multiple Regression of Distance
Matrices based on the biophysical model.
Appendix S3 Full acknowledgements.
Appendix S1.
Sampled locations for each species and related genetic diversity and demographic statistics: nucleotide diversity, π; haplotype diversity, Hd;
effective number of haplotypes, He; number of private haplotypes, Hp; Tajima’s D; and Fu’s Fs. Significance of demographic statistics denoted by
asterisks: *P < 0.05, **P < 0.01, ***P < 0.001.
Species/Location
Longitude, latitude
n
π
Hd
He
Hp
D
Fs
Pomacentrus coelestis
NIN
Ningaloo reef
113.98°E, 21.73°S
24
0.0150
0.9964
22.15
19
-1.47
-22.06***
ASH
Ashmore reef
123.13°E, 12.24°S
32
0.0151
0.9839
21.33
21
-1.04
-23.38***
TIM
Timor l'este
126.42°E, 8.30°S
19
0.0198
0.9649
11.65
12
-1.20
-6.94**
WIG
Wigram Island
136.57°E, 11.76°S
16
0.0141
0.9417
8.53
7
-0.95
-4.59*
Lizard Island
145.49°E, 14.69°S
16
0.0120
0.9619
9.78
5
-0.89
-5.53**
MOT
Motupore Island
147.24°E, 9.44°S
15
0.0112
0.9714
10.71
8
-1.36
-8.53***
KAV
Kavieng
150.78°E, 2.57°S
17
0.0110
0.9485
16.00
9
-1.55*
-7.08***
Lihou reef
151.53°E, 17.62°S
11
0.0087
0.9636
8.07
4
-1.01
-4.58**
HER
Heron Island
151.93°E, 23.49°S
20
0.0087
0.9474
10.00
10
-1.76*
-12.89***
MOO
Mooloolaba
153.12°E, 26.64°S
19
0.0136
0.9591
10.94
8
-1.49
-8.07***
LIZ
LIH
SLT
Solitary Islands
153.15°E, 30.32°S
14
0.0100
0.9341
7.54
7
-1.74*
-5.43**
SOL
Solomon Islands
157.41°E, 8.17°S
16
0.0063
0.8250
4.41
8
-1.99*
-4.85**
LDH
Lord Howe Island
159.07°E, 31.52°S
18
0.0114
0.9281
8.10
6
-1.11
-6.10**
Dascyllus trimaculatus
CHA
Chagos archipelago
72.01°E, 6.08°S
18
0.0239
0.9608
10.80
12
-0.30
-1.09
NIN
Ningaloo reef
113.98°E, 21.73°S
15
0.0144
0.9429
8.33
9
-1.06
-4.42*
ASH
Ashmore reef
123.13°E, 12.24°S
17
0.0154
0.9853
13.76
10
-1.21
-7.98
TIM
Timor l'este
126.42°E, 8.30°S
16
0.0142
1.0000
16.00
8
-1.59*
-13.11***
LIZ
Lizard Island
145.49°E, 14.69°S
15
0.0120
0.9619
9.78
5
-0.89
-5.53**
Motupore Island
147.24°E, 9.44°S
16
0.0123
0.9667
10.67
7
-1.17
-6.39**
MOT
KAV
Kavieng
150.78°E, 2.57°S
16
0.0137
1.0000
16.00
8
-1.84*
-13.17***
LIH
Lihou reef
151.53°E, 17.62°S
6
0.0138
0.9333
4.50
3
-1.07
-0.33
SOL
Solomon Islands
157.41°E, 8.17°S
17
0.0141
0.9853
13.76
9
-1.12
-8.60***
Fiji
177.67°E, 16.73°S
5
0.0109
1.0000
5.00
1
-1.19
-1.72
TGA
FIJ
Tonga
175.20°W, 21.18°S
15
0.0149
0.9810
11.84
8
-0.26
-6.11**
COK
Cook Islands
159.78°W, 21.24°S
9
0.0369
0.8333
3.86
5
1.79
2.32
Halihcoeres hortulanus
CHA
Chagos archipelago
72.01°E, 6.08°S
29
0.0091
0.9089
8.17
12
-1.37
-9.26***
ASH
Ashmore reef
123.13°E, 12.24°S
15
0.0189
0.9905
13.24
8
0.22
-7.01**
TIM
Timor l'este
126.42°E, 8.30°S
5
0.0234
1.0000
5.00
2
0.69
-0.57
LIZ
Lizard Island
145.49°E, 14.69°S
15
0.0208
0.9905
13.24
9
0.38
-6.53**
MOT
Motupore Island
147.24°E, 9.44°S
15
0.0194
0.9905
13.24
6
1.35
-6.85**
KAV
Kavieng
150.78°E, 2.57°S
16
0.0237
0.9830
12.80
9
0.04
-4.89*
LIH
Lihou reef
151.53°E, 17.62°S
16
0.0196
0.9750
11.64
8
0.24
-5.71**
SOL
Solomon Islands
157.41°E, 8.17°S
15
0.0162
0.9619
9.78
7
-0.58
-4.09*
Fiji
177.67°E, 16.73°S
5
0.0150
1.0000
5.00
1
-0.45
-1.22
Tonga
175.20°W, 21.18°S
16
0.0168
0.9667
10.67
8
-0.39
-4.82*
FIJ
TGA
Acanthurus triostegus
NIN
Ningaloo reef
113.98°E, 21.73°S
18
0.0046
0.8366
4.77
3
-1.07
-1.30
ASH
Ashmore reef
123.13°E, 12.24°S
15
0.0022
0.7048
2.92
1
-0.95
-1.06
TIM
Timor l'este
126.42°E, 8.30°S
15
0.0058
0.7714
3.57
2
-0.57
0.60
LIZ
Lizard Island
145.49°E, 14.69°S
15
0.0069
0.9143
6.82
5
-0.68
-1.71
MOT
Motupore Island
147.24°E, 9.44°S
7
0.0038
0.8095
3.27
0
-0.77
0.75
KAV
Kavieng
150.78°E, 2.57°S
15
0.0051
0.8190
4.25
3
-1.31
0.24
LIH
Lihou reef
151.53°E, 17.62°S
15
0.0037
0.8857
5.77
4
-1.37
-2.78
SOL
Solomon Islands
157.41°E, 8.17°S
15
0.0047
0.8667
5.23
0
-1.22
-0.92
TUV
Tuvalu
179.20°E, 8.52°S
16
0.0065
0.8250
4.41
3
-0.82
-1.61
FIJ
Fiji
177.67°E, 16.73°S
11
0.0045
0.8727
4.84
3
-1.22
-1.10
TGA
Tonga
175.20°W, 21.18°S
7
0.0067
0.9524
5.44
2
-0.18
-0.93
COK
Cook Islands
159.78°W, 21.24°S
30
0.0045
0.8345
5.17
6
-1.38
-1.41
Hawaii
158.00°W, 21.41°N
11
0.0053
0.9455
7.12
8
0.24
-1.86
HAW
Comparative analyses of genetic diversity patterns
Methods
We used MANOVA to analyze differences in genetic diversity and demographic history at the
seven locations where all species were co-sampled (using the R base stats package). ‘Location’
and ‘species’ were used as factors, and nucleotide diversity π, haplotype diversity Hd, effective
number of haplotypes He, number of private haplotypes Hp, Tajima’s D, and Fu’s Fs were our
response variables (see Appendix S1 in Supporting Information). We expected that values
would differ among species, but that the patterns across species would be congruent.
Specifically, we hypothesized that there would be a pattern of higher genetic diversity in
locations closest to the junction of the Indian and Pacific Oceans (i.e. highest values in TIM, ASH,
MOT), and that values for Tajima’s D and Fu’s Fs would decrease away from the this region,
indicative of more recent colonization, population expansion, and no population admixture (i.e.
lowest values in KAV, SOL, LIH; H05).
Results
MANOVA revealed there was no effect of location on the raw, or scaled and centred, genetic
response measures (Pillai’s Trace = 1.67, F6,36 = 1.15, P = 0.2825) but there was a significant
effect of species (Pillai’s Trace = 2.17, F3,18 = 6.56, P < 0.0001). Most of the variables were
suitably correlated for MANOVA (i.e. r = 0.20 - 0.60, Meyers et al. 2006), however Hd was
excluded from the MANOVA analysis as it was highly correlated with π and He (r > 0.75) and did
not have a normal distribution following transformation. Some response measures were also
negatively correlated with each other. This is expected given the way that the different genetic
measures are derived, but can interfere with the performance of a MANOVA. Therefore, we
additionally performed two-factor univariate analyses of variance. The univariate relationships
confirmed that species had an effect on all the genetic measures, but also indicated that values
for Tajima’s D varied consistently across species for some locations (F6,18 = 2.77, P = 0.0435). A
Tukey’s test for Honestly Significant Differences revealed that this result was driven by two
significant pairwise relationships among locations; KAV had significantly lower values for
Tajima’s D than both LIZ and MOT (after Tukey’s test: LIZ-KAV, diff = 2.076, P = 0.0140; MOTKAV = 1.992, P = 0.0200). Other than this result, there was little quantitative support for our
prediction that values of genetic diversity and demographic measures would decrease away
from the junction of the Indian and Pacific Oceans (H05).
Discussion
MANOVA suggested there were no differences among statistical estimates of genetic diversity
across the co-sampled study region (P > 0.05). The single exception was Tajima’s D. Tajima’s D
behaved as we predicted: significantly lower values were found at a location most distant from
the junction of the Indian and Pacific Oceans (H05). The low values for Tajima’s D suggest that
all four reef fish species have a relatively recent and isolated population history in Kavieng. Few
studies have included Kavieng in their genetic surveys. Although Barber et al. (2006) found a
divergent lineage that was shared with the northern part of mainland Papua New Guinea in
three stomatopod species, only one of these species had a signature of population expansion.
References
Barber, P. H., Erdmann, M. V., & Palumbi, S. R. (2006) Comparative phylogeography of three
codistributed stomatopods: origins and timing of regional lineage diversification in the coral
triangle. Evolution, 60, 1825–1839.
Meyers, L. S., Gamst, G., & Guarino, A. J. (2006) Applied multivariate research: Design and
interpretation. Sage Publication, Thousand Oaks, CA.
Appendix S2.
Biological parameters for each species used in biophysical models of ‘dispersal distance’.
Biological parameters were selected from published literature where possible, or were
nominated based on the expected dispersal characteristics of each species (i.e. ‘Nominated by
authors’). The biological parameters used in the models included: Spawning frequency – ‘year
round’ or ‘lunar’; max. Pelagic Larval Duration (PLD) – max. published larval duration in days;
Competency – the period following which larvae are competent to settle to a reef habitat;
Homing – ‘yes’ or ‘no’, whether larvae actively seek reef habitat using their sensory ability;
Mortality – mortality rate per day.
Species/biological
parameter
Pomacentrus coelestis
Spawning frequency
Max. PLD
Competency
Source
Year round
Kokita, 2004; Thorrold & Milicich, 1990; Milicich &
Doherty, 1994
Kavanagh & Alford 2003; Thresher et al. 1989
Wellington & Victor, 1989
Homing
Mortality
25 days
50% at day 10; 7 to 12
day transition
yes
10%/day
Dascyllus trimaculatus
Spawning frequency
Max. PLD
Competency
Homing
Mortality
Year round
30 days
23 +/- 2 days
no
10%/day
Nominated by authors
Wellington & Victor, 1989
Weersing & Toonen, 2009
Nominated by authors
Nominated by authors
Halihcoeres hortulanus
Spawning frequency
Max. PLD
Competency
Homing
Mortality
Lunar
37 days
25 +/- 5 days
Yes
10%/day
Nominated by authors
Victor, 1986
Nominated by authors
Nominated by authors
Nominated by authors
Acanthurus triostegus
Spawning frequency
Max. PLD
Lunar
70 days
Competency
Homing
25 +/- 5 days
yes
Mortality
10%/day
Nominated by authors
Planes, 1993; Planes et al. 1994; Planes & Fauvelot,
2002; Wilson & McCormick, 1999
Nominated by authors
Planes, 1993; Planes et al. 1994; Planes & Fauvelot,
2002
Nominated by authors
Gerlach et al. 2007
Nominated by authors
Making a predictor matrix for the Multiple Regression of Distance Matrices based
on the biophysical model. The biophysical model (Treml et al. 2012) outputs the
probability that larvae released in one location survive and settle in every other
recipient location. Migration matrices were then converted using log(M−1) to be the
same rank-order as geographic distance (high proportion of settlers then have a short
‘distance’). The average of the asymmetrical migration matrices was used as the
predictor matrix.
References
Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P., & Miller-Sims, V. (2007) Smelling home
can prevent dispersal of reef fish larvae. Proceedings of the National Academy of Sciences,
104, 858–863.
Kavanagh, K. D., & Alford, R. A. (2003) Sensory and skeletal development and growth in
relation to the duration of the embryonic and larval stages in damselfishes
(Pomacentridae). Biological Journal of the Linnean Society, 80, 187–206.
Kokita, T. (2004) Latitudinal compensation in female reproductive rate of a
geographically widespread reef fish. Environmental Biology of Fishes, 71, 213–224.
Milicich, M. M., & Doherty, P. P. (1994) Larval supply of coral reef fish populations:
magnitude and synchrony of replenishment to Lizard Island, Great Barrier Reef. Marine
Ecology Progress Series, 110, 121–134.
Planes, S. (1993) Genetic differentiation in relation to restricted larval dispersal of the
convict surgeonfish, Acanthurus triostegus, in French Polynesia. Marine Ecology Progress
Series, 98, 237–246.
Planes, S., & Fauvelot, C. (2002) Isolation by distance and vicariance drive genetic
structure of a coral reef fish in the Pacific Ocean. Evolution, 56, 378–399
Planes, S., Borsa, P., Galzin, R., & Bonhomme, F. (1994) Geographic structure and gene
flow in the Manini (convict surgeonfish, Acanthurus triostegus) in South Central Pacific.
Genetics and evolution of aquatic organisms (ed. by A. R. Beaumont), pp 113-122.
Chapman & Hall, London.
Thorrold, S. R., & Milicich, M. J. (1990) Comparison of larval duration and pre-and postsettlement growth in two species of damselfish, Chromis atripectoralis and Pomacentrus
coelestis (Pisces: Pomacentridae), from the Great Barrier Reef. Marine Biology, 105, 375–
384.
Treml, E. A., Roberts, J., Chao, Y., Halpin, P. N., Possingham, H. P., & Riginos, C. (2012)
Reproductive output and duration of the pelagic larval stage determine seascape-wide
connectivity of marine populations. Integrative and Comparative Biology, 52, 525–537.
Thresher, R. E., Colin, P. L., & Bell, L. J. (1989) Planktonic duration, distribution and
population structure of western and central Pacific damselfishes (Pomacentridae).
Copeia, 420–434.
Victor, B. C. (1986) Duration of planktonic larval stage of one hundred species of Pacific
and Atlantic wrasses (family Labridae). Marine Biology, 90, 317–326.
Weersing, K. & Toonen, R. J. (2009) Population genetics, larval dispersal, and
connectivity in marine systems. Marine Ecology Progress Series, 393, 1–12.
Wellington, G. M., & Victor, B. C. (1989) Planktonic larval duration of one hundred
species of Pacific and Atlantic damselfishes (Pomacentridae). Marine Biology, 101, 557–
567.
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Appendix S3. Full acknowledgements
All fish sampling was undertaken with the authority of The University of Queensland
Animal Ethics Committee (Approval Number: SIB/817/08/ARC). Sampling in TimorLeste was supported by the Coral Triangle Support Partnership and the Ministério da
Aquicultura e Pescas, Direcção Nacional de Pescas e Aquicultura (authorised by A
Fernandes, L Fontes, J Freitas; guia de marssa: 502/DNPA/VIII/10 and
452/DNPA/VII/11). Export of samples was authorised by the Departmento de
Quarentena das Pescas (export permit: 162/FQ006/EXP./DNQB/VII/2011). Sampling in
the Solomon Islands was via the Australian Government’s Pacific Strategy Assistance
Program and with the assistance of the Roviana Conservation Foundation (Solomon
Islands Government Ministry of Education & Human Resource Development and
Ministry of Fisheries & Marine Resources research permit to S Albert). Sampling in
Papua New Guinea was in coordination with the National Research Institute, the
Department of Foreign Affairs and Immigration (Research Visa: 10350008304) and the
Department of Environment and Conservation (Permit to Export Wildlife: 011318).
Authority to sample at Ashmore Reef was provided by the Australian Government
Department of Sustainability, Environment, Water, Population & Communities (Access
to Biological Resources in a Commonwealth Area for Non-Commercial Purposes permit
number: AU-COM2010068) and with logistic support from Australian Customs and
border control. Sampling in the Coral Sea was supported by the Marine Division of the
Australian Government Department of Sustainability, Environment, Water, Population &
Communities (Access to Biological Resources in a Commonwealth Area for NonCommercial Purposes permit number: AU-COM2008042). Authority to sample at
Wigram Island was provided by the Northern Territory Government Department of
Resources (Special Permit Number: 2007-2008/S17/2696). Sampling at Ningaloo Reef
was under the authority of the Western Australia Department of Environment &
Conservation (License to take Fauna for Scientific Purposes: SF007126, SF006619;
Authority to enter calm land/or waters: CE002227, CE002627). We are grateful to DJ
Booth and W Figueira for providing samples from New South Wales. We are grateful to B
Bowen for providing samples from Oahu and the Cook Islands. Sampling in Tonga was
under the authority of the Ministry of Agriculture, Food, Forests, and Fisheries (permit
issued to J Drew, Ref: F1/37/09, MOFISH (CAB) 02/09). Sampling in Tuvalu was under
the authority of the Ministry of Natural Resources and Environment (permit issued to J
Drew). Sampling in Fiji was under the authority of the Government of Fiji with a
Ministry of Primary Industries Fisheries Department permit: C564/2009. For sampling
on the Chagos Archipelago, we thank M Gaither, C Sheppard, J Turner, and D Wagner, the
California Academy of Sciences, The Darwin Foundation, The Chagos Conservation
Trust, BIOT Administration and CCT for permitting and facilitating the expedition. We
are grateful to the staff of the Australian Museum Lizard Island Research Station and
Heron Island Research Station for their facilities and support (Great Barrier Reef Marine
Park Authority and Queensland Parks and Wildlife Marine Parks Permit: G08/28114.1,
G09/31678.1, G10/33597.1, G11/34640.1; Queensland Government Department of
Primary Industries General Fisheries Permit: 118636, 150981; Australian Quarantine
Inspection Service Permit to Import Quarantine Material: IP10017966). We especially
thank JD Aguirre, J Aini (Ailan Awareness), S Albert, K Davis, M Jimuru, J Keyse, J Kinch
(National Fisheries College, Papua New Guinea), W Lovell (Freeflow Dive, Dili), I
McLeod, A Mirams, S Penny, R Pinto (and staff of the Coral Triangle Support
Partnership), A Smith (Tiki2 Adventure Tours), T Sinclair-Taylor, A Turner, P Waldie,
MX Weber, Stephen, Lavud, and Takenda for logistical support and field assistance, and J
Hannan and JD Aguirre for images of the study species.