Introduction: The factors shaping vertebrate brain evolution and cognition are broadly categorized as being either social or environmental. Yet, their relative importance is debated, partly due to the limitations associated with standard interspecific evolutionary comparisons. Here, we adopt a complementary strategy leveraging within-population variation in fish brain size to ask how variation in social and environmental factors correlates with individual brain size. Methods: We investigated how overall brain size and brain part sizes varied between demes of the same population in the coral reef-associated batu coris Coris batuensis. This species is ideal for our approach because its local population densities are dissociated from both interspecific densities and habitat complexity. Results: We found that individuals from demes with higher population densities possess larger overall brain volumes than those from lower population density environments, caused by an enlargement of all five main brain regions. Brain anatomical measures show no correlation with interspecific density or habitat complexity. Conclusion: Our results suggest that variation in intraspecific social challenges is selected on individual batu coris brain size, either through phenotypic plasticity, differential survival, or habitat choice. These results conform with a broader version of the social brain hypothesis, emphasizing the importance of the entire brain over specific regions like the neocortex in mammals or the telencephalon in fishes.

1.
Deaner
RO
,
Isler
K
,
Burkart
J
,
Van Schaik
C
.
Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates
.
Brain Behav Evol
.
2007
;
70
(
2
):
115
24
.
2.
Herculano-Houzel
S
,
Messeder
DJ
,
Fonseca-Azevedo
K
,
Pantoja
NA
.
When larger brains do not have more neurons: increased numbers of cells are compensated by decreased average cell size across mouse individuals
.
Front Neuroanat
.
2015
;
9
:
64
.
3.
Logan
CJ
,
Avin
S
,
Boogert
N
,
Buskell
A
,
Cross
FR
,
Currie
A
, et al
.
Beyond brain size: uncovering the neural correlates of behavioral and cognitive specialization
.
Comp Cogn Behav Rev
.
2018
;
13
:
55
89
.
4.
Byrne
RW
,
Whiten
A
.
Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans
.
Oxford University Press
;
1988
.
5.
Dunbar
RIM
.
The social brain hypothesis
.
Evol Anthropol
.
1998
;
6
(
5
):
178
90
.
6.
Humphrey
NK
.
The social function of intellect
.
Growing points in ethology
.
1976
; p.
303
17
.
7.
Whiten
A
.
Social, Machiavellian and cultural cognition: a golden age of discovery in comparative and evolutionary psychology
.
J Comp Psychol
.
2018
;
132
(
4
):
437
41
.
8.
Clutton-Brock
TH
,
Harvey
PH
.
Primate ecology and social organization
.
J Zool
.
1977
;
183
:
1
39
.
9.
Iwaniuk
AN
,
Nelson
JE
.
A comparative analysis of relative brain size in waterfowl (anseriformes)
.
Brain Behav Evol
.
2001
;
57
(
2
):
87
97
.
10.
DeCasien
AR
,
Williams
SA
,
Higham
JP
.
Primate brain size is predicted by diet but not sociality
.
Nat Ecol Evol
.
2017
;
1
(
5
):
112
.
11.
Rosati
AG
.
Foraging cognition: reviving the ecological intelligence hypothesis
.
Trends Cogn Sci
.
2017
;
21
(
9
):
691
702
.
12.
Oliveira
RF
,
Bshary
R
.
Expanding the concept of social behavior to interspecific interactions
.
Ethology
.
2021
;
127
(
10
):
758
73
.
13.
Aiello
LC
,
Wheeler
P
.
The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution
.
Curr Anthropol
.
1995
;
2
:
557
60
.
14.
Isler
K
,
van Schaik
C
.
Costs of encephalization: the energy trade-off hypothesis tested on birds
.
J Hum Evol
.
2006
;
51
(
3
):
228
43
.
15.
Heldstab
SA
,
Isler
K
,
Graber
SM
,
Schuppli
C
,
van Schaik
CP
.
The economics of brain size evolution in vertebrates
.
Curr Biol
.
2022
;
32
(
12
):
R697
708
.
16.
Healy
SD
,
Rowe
C
.
A critique of comparative studies of brain size
.
Proc Biol Sci
.
2007
;
274
(
1609
):
453
64
.
17.
Gonda
A
,
Herczeg
G
,
Merilä
J
.
Evolutionary ecology of intraspecific brain size variation: a review
.
Ecol Evol
.
2013
;
3
(
8
):
2751
64
.
18.
Hall
ZJ
,
Tropepe
V
.
Using teleost fish to discern developmental signatures of evolutionary adaptation from phenotypic plasticity in brain structure
.
Front Neuroanat
.
2020
;
14
:
10
.
19.
Ishikawa
Y
,
Yoshimoto
M
,
Yamamoto
N
,
Ito
H
.
Different brain morphologies from different genotypes in a single teleost species, the medaka (Oryzias latipes)
.
Brain Behav Evol
.
1999
;
53
(
1
):
2
9
.
20.
Axelrod
CJ
,
Laberge
F
,
Robinson
BW
.
Intraspecific brain size variation between coexisting sunfish ecotypes
.
Proc Biol Sci
.
2018
;
285
(
1890
):
20181971
.
21.
Reyes
AS
,
Bittar
A
,
Ávila
LC
,
Botia
C
,
Esmeral
NP
,
Bloch
NI
.
Divergence in brain size and brain region volumes across wild guppy populations
.
Proc Biol Sci
.
2022
;
289
(
1981
):
20212784
.
22.
Pravosudov
VV
,
Roth II
TC
.
Cognitive ecology of food hoarding: the evolution of spatial memory and the hippocampus
.
Annu Rev Ecol Evol Syst
.
2013
;
44
(
1
):
173
93
.
23.
Zupanc
GKH
,
Horschke
I
.
Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study
.
J Comp Neurol
.
1995
;
353
(
2
):
213
33
.
24.
Zupanc
GKH
.
Neurogenesis and neuronal regeneration in the adult fish brain
.
J Comp Physiol A
.
2006
;
192
(
6
):
649
70
.
25.
Kihslinger
RL
,
Nevitt
GA
.
Early rearing environment impacts cerebellar growth in juvenile salmon
.
J Exp Biol
.
2006
;
209
(
Pt 3
):
504
9
.
26.
Burns
JG
,
Saravanan
A
,
Helen Rodd
F
.
Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies
.
Ethology
.
2009
;
115
(
2
):
122
33
.
27.
Gonda
A
,
Herczeg
G
,
Merilä
J
.
Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius): local adaptation or environmentally induced variation
.
BMC Evol Biol
.
2011
;
11
:
75
.
28.
Bshary
R
,
Triki
Z
.
Fish ecology and cognition: insights from studies on wild and wild-caught teleost fishes
.
Curr Opin Behav Sci
.
2022
;
46
:
101174
.
29.
Fong
S
,
Buechel
SD
,
Boussard
A
,
Kotrschal
A
,
Kolm
N
.
Plastic changes in brain morphology in relation to learning and environmental enrichment in the guppy (Poecilia reticulata)
.
J Exp Biol
.
2019
;
222
(
Pt 10
):
jeb200402
.
30.
Triki
Z
,
Levorato
E
,
McNeely
W
,
Marshall
J
,
Bshary
R
.
Population densities predict forebrain size variation in the cleaner fish Labroides dimidiatus
.
Proc Biol Sci
.
2019
;
286
(
1915
):
20192108
.
31.
Triki
Z
,
Emery
Y
,
Teles
MC
,
Oliveira
RF
,
Bshary
R
.
Brain morphology predicts social intelligence in wild cleaner fish
.
Nat Commun
.
2020
;
11
:
6423
9
.
32.
Gardner
MJ
,
Chaplin
JA
,
Potter
IC
,
Fairclough
DV
.
Pelagic early life stages promote connectivity in the demersal labrid Choerodon rubescens
.
J Exp Mar Biol Ecol
.
2015
;
472
:
142
50
.
33.
Jones
DB
,
Jerry
DR
,
McCormick
MI
,
Bay
LK
.
The population genetic structure of a common tropical damselfish on the Great Barrier Reef and Eastern Papua New Guinea
.
Coral Reefs
.
2010
;
29
(
2
):
455
67
.
34.
Knutsen
H
,
Catarino
D
,
Rogers
L
,
Sodeland
M
,
Mattingsdal
M
,
Jahnke
M
, et al
.
Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species
.
Mol Ecol
.
2022
;
31
(
9
):
2562
77
.
35.
Victor
BC
.
Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (family Labridae)
.
Mar Biol
.
1986
;
90
(
3
):
317
26
.
36.
Côté
I
.
Evolution and ecology of cleaning symbioses in the sea
.
Oceanogr Mar Biol
.
2000
;
38
:
311
.
37.
Grutter
AS
,
Bshary
R
.
Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions
.
Proc Biol Sci
.
2003
;
270
(
Suppl 2
):
S242
4
.
38.
Bshary
R
,
Grutter
AS
.
Image scoring and cooperation in a cleaner fish mutualism
.
Nature
.
2006
;
441
(
7096
):
975
8
.
39.
Binning
SA
,
Rey
O
,
Wismer
S
,
Triki
Z
,
Glauser
G
,
Soares
MC
, et al
.
Reputation management promotes strategic adjustment of service quality in cleaner wrasse
.
Sci Rep
.
2017
;
7
:
8425
9
.
40.
Bshary
R
,
Würth
M
.
Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation
.
Proc R Soc Lond B
.
2001
;
268
(
1475
):
1495
501
.
41.
Wismer
S
,
Pinto
AI
,
Vail
AL
,
Grutter
AS
,
Bshary
R
.
Variation in cleaner wrasse cooperation and cognition: influence of the developmental environment
.
Ethology
.
2014
;
120
(
6
):
519
31
.
42.
Triki
Z
,
Wismer
S
,
Rey
O
,
Ann Binning
S
,
Levorato
E
,
Bshary
R
.
Biological market effects predict cleaner fish strategic sophistication
.
Behav Ecol
.
2019
;
30
(
6
):
1548
57
.
43.
Wismer
S
,
Pinto
AI
,
Triki
Z
,
Grutter
AS
,
Roche
DG
,
Bshary
R
.
Cue-based decision rules of cleaner fish in a biological market task
.
Anim Behav
.
2019
;
158
:
249
60
.
44.
Kuwamura
T
,
Sawada
K
,
Sunobe
T
,
Sakai
Y
,
Kadota
T
.
Hermaphroditism and mating systems in fish
.
Singapore
:
Springer Nature Singapore
;
2023
.
45.
Ryen
CA
.
Sex-specific growth dynamics in protogynous hermaphrodites
.
2007
.
46.
Randall
JE
.
Revision of the Indo-Pacific labrid fishes of the genus Coris, with descriptions of five new species
.
Bernice Pauahi Bishop Mus
.
1999
.
47.
Kramer
MJ
,
Bellwood
O
,
Bellwood
DR
.
Foraging and microhabitat use by crustacean-feeding wrasses on Coral Reefs
.
Mar Ecol Prog Ser
.
2016
;
548
:
277
82
.
48.
Green
AL
.
Spatial, temporal and ontogenetic patterns of habitat use by coral reef fishes (Family Labridae)
.
Mar Ecol Prog Ser
.
1996
;
133
:
1
11
.
49.
Triki
Z
,
Bshary
R
.
Fluctuations in coral reef fish densities after environmental disturbances on the Northern Great Barrier Reef
.
PeerJ
.
2019
;
7
:
e6720
.
50.
Krattinger
O
.
A phylogenetic comparison of cleaning behaviour and morphology in wrasses
.
2016
.
51.
Ryen
C
.
Sex-specific growth dynamics in protogynous hermaphrodites
.
2007
.
52.
Darling
ES
,
Graham
NAJ
,
Januchowski-Hartley
FA
,
Nash
KL
,
Pratchett
MS
,
Wilson
SK
.
Relationships between structural complexity, coral traits, and reef fish assemblages
.
Coral Reefs
.
2017
;
36
(
2
):
561
75
.
53.
White
GE
,
Brown
C
.
Variation in brain morphology of intertidal gobies: a comparison of methodologies used to quantitatively assess brain volumes in fish
.
Brain Behav Evol
.
2015
;
85
(
4
):
245
56
.
54.
Pollen
AA
,
Dobberfuhl
AP
,
Scace
J
,
Igulu
MM
,
Renn
SCP
,
Shumway
CA
, et al
.
Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish
.
Brain Behav Evol
.
2007
;
70
(
1
):
21
39
.
55.
Huxley
JS
.
Constant differential growth-ratios and their significance
.
Nature
.
1924
;
114
(
2877
):
895
6
.
56.
Kerkhoff
AJ
,
Enquist
BJ
.
Multiplicative by nature: why logarithmic transformation is necessary in allometry
.
J Theor Biol
.
2009
;
257
(
3
):
519
21
.
57.
Pélabon
C
,
Tidière
M
,
Lemaître
J-F
,
Gaillard
J-M
.
Modelling allometry: statistical and biological considerations – a reply to Packard
.
Biol J Linn Soc Lond
.
2018
.
58.
Dunbar
RIM
.
Neocortex size as a constraint on group size in primates
.
J Hum Evol
.
1992
;
22
(
6
):
469
93
.
59.
Emery
NJ
,
Seed
AM
,
von Bayern
AMP
,
Clayton
NS
.
Cognitive adaptations of social bonding in birds
.
Philos Trans R Soc Lond B Biol Sci
.
2007
;
362
(
1480
):
489
505
.
60.
Zuberbühler
K
,
Byrne
RW
.
Social cognition
.
Curr Biol
.
2006
;
16
(
18
):
R786
90
.
61.
Wilson
DT
,
McCormick
MI
.
Microstructure of settlement-marks in the otoliths of tropical reef fishes
.
Mar Biol
.
1999
;
134
(
1
):
29
41
.
62.
Green
AL
.
Spatio-temporal patterns of recruitment of labroid fishes (Pisces: Labridae and Scaridae) to damselfish territories
.
Environ Biol Fishes
.
1998
;
51
(
3
):
235
44
.
63.
Streit
RP
,
Bellwood
DR
.
High prevalence of homing behaviour among juvenile coral-reef fishes and the role of body size
.
Coral Reefs
.
2017
;
36
(
4
):
1083
95
.
64.
Goodson
JL
.
The vertebrate social behavior network: evolutionary themes and variations
.
Horm Behav
.
2005
;
48
(
1
):
11
22
.
65.
O’Connell
LA
,
Hofmann
HA
.
Evolution of a vertebrate social decision-making network
.
Science
.
2012
;
336
(
6085
):
1154
7
.
66.
O’Connell
LA
,
Hofmann
HA
.
The Vertebrate mesolimbic reward system and social behavior network: a comparative synthesis
.
J Comp Neurol
.
2011
;
519
(
18
):
3599
639
.
67.
Finlay
BL
,
Darlington
RB
.
Linked regularities in the development and evolution of mammalian brains
.
Science
.
1995
;
268
(
5217
):
1578
84
.
68.
Kozol
RA
,
Conith
AJ
,
Yuiska
A
,
Cree-Newman
A
,
Tolentino
B
,
Benesh
K
, et al
.
A brain-wide analysis maps structural evolution to distinct anatomical module
.
Elife
.
2023
;
12
:
e80777
.
69.
Mahabir
PN
,
Billotte
C
,
Gutgesell
MK
,
Guzzo
MM
,
McCann
KS
,
Bernier
NJ
, et al
.
Brain form and foraging behaviour in a stream fish
.
Environ Biol Fishes
.
2024
;
107
(
7
):
771
84
.
70.
Schumacher
EL
,
Carlson
BA
.
Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes
.
Elife
.
2022
;
11
:
e74159
.
71.
Sukhum
KV
,
Shen
J
,
Carlson
BA
.
Extreme enlargement of the cerebellum in a clade of teleost fishes that evolved a novel active sensory system
.
Curr Biol
.
2018
;
28
(
23
):
3857
63.e3
.
72.
Gonzalez-Voyer
A
,
Winberg
S
,
Kolm
N
.
Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes
.
BMC Evol Biol
.
2009
;
9
:
238
.
73.
van Schaik
CP
,
Song
Z
,
Schuppli
C
,
Drobniak
SM
,
Heldstab
SA
,
Griesser
M
.
Extended parental provisioning and variation in vertebrate brain sizes
.
PLoS Biol
.
2023
;
21
(
2
):
e3002016
.
74.
Barton
RA
.
From the cover: binocularity and brain evolution in primates
.
Proc Natl Acad Sci U S A
.
2004
;
101
(
27
):
10113
5
.
75.
De Meester
G
,
Huyghe
K
,
Van Damme
R
.
Brain size, ecology and sociality: a reptilian perspective
.
Biol J Linn Soc Lond
.
2019
;
126
(
3
):
381
91
.
76.
Barton
RA
.
Embodied cognitive evolution and the cerebellum
.
Philos Trans R Soc Lond B Biol Sci
.
2012
;
367
(
1599
):
2097
107
.
77.
Fricke
HW
.
Control of different mating systems in a coral reef fish by one environmental factor
.
Anim Behav
.
1980
;
28
(
2
):
561
9
.
78.
Lutnesky
MMF
.
Density-dependent protogynous sex change in territorial-haremic fishes: models and evidence
.
Behav Ecol
.
1994
;
5
(
4
):
375
83
.
79.
van Rooij
JM
,
Kok
JP
,
Videler
JJ
.
Local variability in population structure and density of the protogynous reef herbivore Sparisoma viride
.
Environ Biol Fishes
.
1996
;
47
(
1
):
65
80
.
80.
Mumby
PJ
,
Wabnitz
CCC
.
Spatial patterns of aggression, territory size, and harem size in five sympatric caribbean parrotfish species
.
Environ Biol Fishes
.
2002
;
63
(
3
):
265
79
.
81.
Warner
RR
,
Hoffman
SG
.
Local population size as a determinant of mating system and sexual composition in two tropical marine fishes (Thalassoma spp.)
.
Evol
.
1980
;
34
(
3
):
508
18
.
82.
Taborsky
B
,
Oliveira
RF
.
Social competence: an evolutionary approach
.
Trends Ecol Evol
.
2012
;
27
(
12
):
679
88
.
83.
Randall
JE
,
Allen
GR
,
Steene
RC
.
Fishes of the great barrier reef and coral sea
.
University of Hawaii Press
;
1998
.
84.
Isler
K
,
van Schaik
CP
.
The Expensive Brain: a framework for explaining evolutionary changes in brain size
.
J Hum Evol
.
2009
;
57
(
4
):
392
400
.
85.
Gingins
S
,
Bshary
R
.
The cleaner wrasse outperforms other labrids in ecologically relevant contexts, but not in spatial discrimination
.
Anim Behav
.
2016
;
115
:
145
55
.
86.
Salwiczek
LH
,
Prétôt
L
,
Demarta
L
,
Proctor
D
,
Essler
J
,
Pinto
AI
, et al
.
Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner: client reef fish cooperation
.
PLoS One
.
2012
;
7
(
11
):
e49068
.
87.
Zentall
TR
,
Case
JP
,
Luong
J
.
Pigeon’s (Columba livia) paradoxical preference for the suboptimal alternative in a complex foraging task
.
J Comp Psychol
.
2016
;
130
(
2
):
138
44
.
88.
Emery
Y
,
Pessina
L
,
Bshary
R
.
Population density affects whole brain and brain region volumes in a wrasse species Coris batuensis
.
EcoEvoRxiv
.
2023
. preprint: not peer reviewed.
89.
Emery
Y
,
Pessina
L
,
Bshary
R
.
Data from: population density affects whole brain and brain region volumes in a wrasse species Coris batuensis
.
You do not currently have access to this content.