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Supplementary Material
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Environmental stability and the evolution of cooperative breeding
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in hornbills
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Juan-Carlos T. Gonzalez, Ben C. Sheldon and Joseph A. Tobias
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Contents
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Supplementary methods
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Supplementary figures (S1)
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Data tables (S1–S2)
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Results tables (S3–S4)
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Supplementary methods
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Testing for co-evolution between cooperative breeding and other intrinsic traits
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We reconstructed the evolution of cooperative breeding in 25 cooperatively
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breeding species of hornbill using the module DISCRETE [1] of BAYESTRAITS
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[2]. This method determines whether two traits are more likely to have evolved in
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tandem on the basis of the frequency of transitions between the different combined
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states. It first reconstructs the most likely scenario if two traits evolved
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independently in the phylogenetic tree and compares this with a scenario in which
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the two traits are linked in the four possible combinations and where the transitions
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occur at random. The evolution of characters across the phylogeny was
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reconstructed assuming both independent and dependent evolution of the two states.
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Significance of results was measured by performing a likelihood ratio test,
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comparing twice the difference between the independent and dependent model to a
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chi-square test with four degrees of freedom to reflect the higher number of
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parameters in the dependent model.
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Additional phylogenetic comparative analyses
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We tested whether our results were robust to alternative phylogenetic modelling
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approaches by conducting phylogenetic independent contrasts (PIC) and
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phylogenetic-generalized least squares (PGLS) analyses. PICs corrected for branch
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length were generated using the function ‘pic’ of the package APE [3] in R, using a
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recently published phylogeny of hornbills [4]. The contrasts of all intrinsic and
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extrinsic variables were tested against contrasts in cooperative breeding in linear
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regressions in which the intercept is forced to pass through zero (using the ‘lm’
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function in R). PGLS, meanwhile, uses maximum likelihood to estimate the most
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likely transformation of branch lengths according to Pagel’s lambda to explain the
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evolution of cooperative breeding while assessing an association with potential
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predictors. PGLS analyses were implemented using the package ‘CAPER’ [5] in R.
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Supplementary Figures
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Figure S1. The relationship between social system and body mass for (a)
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cooperative breeding hornbills (n = 25) and (b) non-cooperative hornbills (n = 36).
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Sources for mass data are given in table S1. Tukey box plots summarise these data
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for a single axis.
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Supplementary Tables
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Table S1. Social system and ecological traits of hornbills
Social
Preferred
Primary
Terri-
Nest
Body
system
habitat
diet
toriality
hole
mass
Aceros cassidix
Non
Humid
Frug
NonT
1049
2360
Aceros nipalensis
Non
Humid
Frug
NonT
350a
2385
Anorrhinus austeni
Coop
Humid
Frug
Terr
350a
1079.5
Anorrhinus galeritus
Coop
Humid
Frug
Terr
195
1172
Anorrhinus tickelli
Coop
Humid
Frug
Terr
350a
792.6
Anthracoceros albirostris
Non
Humid
Frug
Terr
226
892.9
Anthracoceros coronatus
Non
Humid
Frug
Terr
350a
806.7
Anthracoceros malayanus
Coop
Humid
Frug
Terr
350a
1050
Anthracoceros marchei
Coop
Humid
Frug
Terr
350a
750
Anthracoceros montani
Coop
Humid
Frug
Terr
200a
714.6
Berenicornis comatus
Coop
Humid
Frug
Terr
350a
1470
Buceros bicornis
Non
Humid
Frug
NonT
567
2790.8
Buceros hydrocorax
Coop
Humid
Frug
NonT
385
1409.6
Buceros rhinoceros
Coop
Humid
Frug
NonT
600a
2371.6
Bucorvus abyssinicus
Coop
Dry
NonF
Terr
600a
4000
Bucorvus leadbeateri
Coop
Dry
NonF
Terr
600a
3743.6
Bycanistes albotibialis
Non
Humid
Frug
NonT
350a
1137.8
Bycanistes brevis
Non
Dry
Frug
NonT
350a
1232.8
Bycanistes bucinator
Coop
Dry
Frug
NonT
200a
639.4
Bycanistes cylindricus
Non
Humid
Frug
NonT
98
921
Bycanistes fistulator
Coop
Humid
Frug
NonT
115a
508.1
Bycanistes subcylindricus
Coop
Humid
Frug
NonT
350a
1195.4
Ceratogymna atrata
Coop
Humid
Frug
NonT
130
1194.8
Ceratogymna elata
Coop
Humid
Frug
NonT
350a
1917
Lophoceros alboterminatus
Non
Humid
Frug
Terr
115a
223.7
Taxon
Lophoceros bradfieldi
Non
Dry
NonF
Terr
115a
196.5
Lophoceros camurus
Coop
Humid
NonF
Terr
115a
103.8
Lophoceros fasciatus
Non
Humid
Frug
Terr
115a
258.8
Lophoceros hemprichii
Non
Dry
NonF
Terr
200a
297
Lophoceros nasutus
Non
Dry
NonF
Terr
200a
179.6
Lophoceros pallidirostris
Non
Dry
NonF
Terr
115a
233
Ocyceros birostris
Coop
Dry
Frug
Terr
115a
375
Ocyceros gingalensis
Coop
Humid
Frug
Terr
115a
238
Ocyceros griseus
Non
Humid
Frug
Terr
70
292
Penelopides affinis
Coop
Humid
Frug
Terr
200a
456
Penelopides manillae
Coop
Humid
Frug
Terr
176
460.9
Penelopides mindorensis
Coop
Humid
Frug
Terr
200a
462
Penelopides panini
Coop
Humid
Frug
Terr
169
470.5
Penelopides samarensis
Coop
Humid
Frug
Terr
200a
478.4
Rhabdotorrhinus corrugatus
Non
Humid
Frug
NonT
350a
1590
Rhabdotorrhinus exarhatus
Coop
Humid
Frug
Terr
300a
370
Rhabdotorrhinus leucocephalus
Non
Humid
Frug
NonT
350a
1086
Rhabdotorrhinus waldeni
Non
Humid
Frug
NonT
350a
1748.8
Rhinoplax vigil
Non
Humid
Frug
Terr
600a
2887.6
Rhyticeros everetti
Non
Humid
Frug
NonT
672
1748.8
Rhyticeros narcondami
Non
Humid
Frug
NonT
756
697.2
Rhyticeros plicatus
Non
Humid
Frug
NonT
350a
1703.8
Rhyticeros subruficollis
Non
Humid
Frug
NonT
350a
2042
Rhyticeros undulatus
Non
Humid
Frug
NonT
324
2214.6
Tockus damarensis
Non
Dry
NonF
Terr
115a
192.5
Tockus deckeni
Non
Dry
NonF
Terr
115a
169.5
Tockus erythrorhynchus
Non
Dry
NonF
Terr
115a
154
Tockus flavirostris
Non
Dry
NonF
Terr
115a
216.7
Tockus jacksoni
Non
Dry
NonF
Terr
115a
167.7
Tockus kempi
Non
Dry
NonF
Terr
115a
138.6
Tockus leucomelas
Non
Dry
NonF
Terr
115a
188.3
Tockus monteiri
Non
Dry
NonF
Terr
144
289.8
Tockus ruahae
Non
Dry
NonF
Terr
115a
126.5
Tockus rufirostris
Non
Dry
NonF
Terr
115a
134.3
Horizocerus albocristatus
Non
Humid
Frug
Terr
200a
289.4
Horizocerus hartlaubi
Non
Humid
NonF
Terr
115a
98.5
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Taxonomy follows Gonzalez et al. [4] with subsequent corrections.
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Abbreviations: Coop: Cooperative breeding; Non: Non-cooperative breeding;
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Humid: Humid forests; Dry: Drylands; Frug: Frugivorous; NonF: Non-
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frugivorous; Terr: Terrtorial; NonT: Non-Territorial.
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Primary sources: Habitat [6, 7]; Diet [6], with updates by [8, 9]; Territoriality [6, 7,
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10, 11]; Nest hole size [12-19], and J. C. Gonzalez, unpublished data; Body mass
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[20].
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a
Data inferred from Galama et al. [21].
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Table S2. Climatic variables extracted from hornbill range polygons by Jetz &
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Rubenstein [22], with data for six other species generated using the same methods.
Mean annual
Temp. var.
Temp. var.
Mean annual
Ppt. var.
Ppt. var.
Taxon
temp.
within years
between years
ppt.
within years
between years
Aceros cassidix
25.3
1.1
1.1
2089.5
1.5
1.1
Aceros nipalensis
21.6
10.5
1.7
1889.7
5.9
1.9
Anorrhinus austeni
23.9
9.8
1.8
1751.8
5.5
1.7
26
1.2
1.1
2734.6
1.3
0.9
Anorrhinus tickelli
23.1
4.3
1.6
1998.4
7.4
2.4
Anthracoceros albirostris
24.8
7
1.6
2169.8
4.5
1.8
Anthracoceros coronatus
26
9.4
1.7
1461.7
9.7
3.8
Anthracoceros malayanus
26
1.1
1.1
2761.1
1.2
0.9
Anthracoceros marchei
26.9
1.9
1.3
2135.1
2.5
1
Anthracoceros montani
26.8
1.1
1.4
1872.5
1.3
1.3
Berenicornis comatus
24.3
1.2
1.2
1584.1
1.5
1
Buceros bicornis
24.6
7.4
1.7
2067.7
5.6
1.9
Buceros hydrocorax
25.9
2.6
1.4
2655.1
2.6
1.2
Buceros rhinoceros
25.9
1.1
1.1
2743.8
1.4
1
Bucorvus abyssinicus
25.3
6.2
1.9
1013.5
12.1
3.6
Bucorvus leadbeateri
21.8
6.8
1.7
961.8
11.3
3.2
Bycanistes albotibialis
24.6
2.8
1.5
1770.7
5.5
1.9
Bycanistes brevis
21.7
5.1
1.5
982.5
5.9
2.4
Bycanistes bucinator
22.1
6.1
1.6
1015.6
10.3
3
Bycanistes cylindricus
25.8
2.5
1.3
2069.3
4.4
1.5
Bycanistes fistulator
24.8
2.8
1.3
1736
5.7
1.7
Bycanistes subcylindricus
23.8
2.8
1.5
1491.9
5.5
1.9
Ceratogymna atrata
24.6
2.4
1.3
1771
4.4
1.4
Ceratogymna elata
26.2
3.4
1.3
2033.9
7.3
2.3
Lophoceros alboterminatus
22.2
5.4
1.5
1033.8
9.1
2.7
Lophoceros bradfieldi
21.6
10.8
2.4
571.2
15.9
4.5
Lophoceros camurus
24.8
2.4
1.3
1836.4
3.8
1.3
Lophoceros fasciatus
25
2.8
1.4
1719.3
5.9
1.8
22.4
4.5
1.7
725.8
6
3.1
Anorrhinus galeritus
Lophoceros hemprichii
Lophoceros nasutus
24.2
7
1.9
830
11.4
3.6
Lophoceros pallidirostris
22.2
5.6
1.5
1182.9
11.9
3.2
Ocyceros birostris
25.6
13.2
1.9
1127.5
9.6
4.3
Ocyceros gingalensis
27.1
3.1
1.5
1755.5
2.4
1.8
Ocyceros griseus
25.8
5.5
1.4
1835.8
12.7
3.9
Penelopides affinis
25.8
1.7
1.4
2650.6
1.4
1
Penelopides manillae
25.9
3.6
1.4
2739.5
4
1.5
Penelopides mindorensis
26.4
2.6
1.4
2421.2
3.8
1.6
Penelopides panini
26.9
2.2
1.2
2448.6
2.1
1.2
Penelopides samarensis
26.5
2.3
1.2
2644.9
1.4
1.1
Rhabdotorrhinus corrugatus
25.9
1.1
1.1
2776.3
1.2
0.9
Rhabdotorrhinus leucocephalus
25.7
1.5
1.5
2697.7
1.4
1
Rhabdotorrhinus exarhatus
24.8
1.1
1.1
2127
1.5
1.1
Rhabdotorrhinus waldeni
26.8
2.1
1.2
2419.5
2.4
1.3
26
1.2
1.1
2754.5
1.3
0.9
25.9
2.3
1.3
2776.3
4.1
1.8
27
2
1.5
2980
4.6
1.9
Rhyticeros plicatus
25.3
1.5
1.5
2856.5
1.1
0.9
Rhyticeros subruficollis
24.7
4.7
1.5
2363.8
7.2
2.5
Rhyticeros undulatus
25.2
5
1.5
2342.6
4
1.5
Tockus damarensis
20.9
9.1
2.1
527.1
13.8
4.8
Tockus deckeni
23.9
3.5
1.5
613.5
7.2
3.3
Tockus erythrorhynchus
24.1
7.8
2
686.5
12.2
4
Tockus flavirostris
24.7
4.5
1.6
480.3
7.1
3.5
Tockus jacksoni
25.5
4.5
1.6
595.3
7.1
3.5
Tockus kempi
26.6
6.2
1.9
266.2
12.1
3.6
Tockus leucomelas
20.9
11.2
2.2
539.6
12.1
4.3
Tockus monteiri
20.4
9.1
2.1
360.3
13.8
4.8
Tockus ruahae
21.2
4.5
1.6
1002
7.1
3.5
Tockus rufirostris
21.3
11.2
2.2
754.7
12.1
4.3
25
2.5
1.3
1860.5
4.1
1.4
24.9
2.3
1.3
1795
3.6
1.2
Rhinoplax vigil
Rhyticeros everetti
Rhyticeros narcondami
Horizocerus albocristatus
Horizocerus hartlaubi
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Table S3. Correlates of cooperative breeding in hornbills using alternative
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phylogenetic modelling approaches
Modelling approach
PGLS
PIC
Variablesa
Estimate ± SE
t
Estimate ± SE
F1,59
Preferred habitat
0.012 ± 0.178
0.065
0.012 ± 0.178
0.004
Primary diet
0.07 ± 0.261
0.268
0.07 ± 0.262
0.072
Territoriality
0.524 ± 0.213
2.464*
0.524 ± 0.213
6.071
Body mass
-0.175 ± 0.097
-1.804
-0.175 ± 0.097
3.254
Mean annual temp.
0.502 ± 0.689
0.729
0.502 ± 0.689
0.532
Mean annual ppt.
0.042 ± 0.137
0.306
0.042 ± 0.137
0.093
Temp. var. within yrs
-0.178 ± 0.075
-2.372*
-0.178 ± 0.075
5.627*
Temp. var. among yrs
-0.517 ± 0.318
-1.628
-0.517 ± 0.318
2.65
Ppt. var. within yrs
-0.179 ± 0.078
-2.289*
-0.179 ± 0.078
5.239*
Ppt. var. among yrs
-0.29 ± 0.127
-2.278*
-0.29 ± 0.127
5.191*
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Bold denotes significant effect of variable on occurrence of cooperative breeding
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74
*p < 0.05
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107
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109
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111
112
113
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