Introduction: Comparative studies of brain anatomy between closely related species have been very useful in demonstrating selective changes in brain structure. Within-species comparisons can be particularly useful for identifying changes in brain structure caused by contrasting environmental selection pressures. Here, we aimed to understand whether differences within and between species in habitat use and foraging behaviour influence brain morphology, on both ecological and evolutionary time scales. Methods: We used as a study model three species of the Elacatinus genus that differ in their habitat-foraging mode. The obligatory cleaning goby Elacatinus evelynae inhabits mainly corals and feeds mostly on ectoparasites removed from larger fish during cleaning interactions. In contrast, the obligatory sponge-dwelling goby Elacatinus chancei inhabits tubular sponges and feeds on microinvertebrates buried in the sponges’ tissues. Finally, in the facultatively cleaning goby Elacatinus prochilos, individuals can adopt either phenotype, the cleaning or the sponge-dwelling habitat-foraging mode. By comparing the brains of the facultative goby phenotypes to the brains of the obligatory species we can test whether brain morphology is better predicted by phylogenetic relatedness or the habitat-foraging modes (cleaning × sponge dwelling). Results: We found that E. prochilos brains from both types (cleaning and sponge dwelling) were highly similar to each other. Their brains were in general more similar to the brains of the most closely related species, E. evelynae (obligatory cleaning species), than to the brains of E. chancei (sponge-dwelling species). In contrast, we found significant brain structure differences between the cleaning species (E. evelynae and E. prochilos) and the sponge-dwelling species (E. chancei). These differences revealed independent changes in functionally correlated brain areas that might be ecologically adaptive. E. evelynae and E. prochilos had a relatively larger visual input processing brain axis and a relatively smaller lateral line input processing brain axis than E. chancei. Conclusion: The similar brain morphology of the two types of E. prochilos corroborates other studies showing that individuals of both types can be highly plastic in their social and foraging behaviours. Our results in the Elacatinus species suggest that morphological adaptations of the brain are likely to be found in specialists whereas species that are more flexible in their habitat may only show behavioural plasticity without showing anatomical differences.

1.
Northcutt
RG
.
Understanding vertebrate brain evolution
.
Integr Comp Biol
.
2002
;
42
(
4
):
743
56
.
2.
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
.
3.
Hofmann
MH
.
Sex differences in the swordtail Xiphophorus hellerii revealed by a new method to investigate volumetric data
.
Biotechnol Bioproc Eng
.
2020
;
95
(
3–4
):
127
38
.
4.
Kotrschal
K
,
Junger
H
.
Patterns of brain morphology in mid-European Cyprinidae (Pisces, Teleostei): a quantitative histological study
.
J Hirnforsch
.
1988
;
29
(
3
):
341
52
.
5.
Brandstätter
R
,
Kotrschal
K
.
Brain growth patterns in four European cyprinid fish species (cyprinidae, teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus)
.
Brain Behav Evol
.
1990
;
35
(
4
):
195
211
.
6.
Kotrschal
K
,
Palzenberger
M
.
Neuroecology of cyprinids: comparative, quantitative histology reveals diverse brain patterns
. In:
Wieser
W
,
Schiemer
F
,
Goldschmidt
A
, et al
, editors.
Environmental biology of European cyprinids
.
Dordrecht
:
Springer Netherlands
;
1992
[cited 2024 Jan 31]. p.
135
52
. Available from: https://link.springer.com/10.1007/978-94-011-2544-4_13
7.
Van Staaden
M
,
Huber
R
,
Kaufman
L
,
Liem
KF
.
Brain evolution in cichlids of the African Great Lakes: brain and body size, general patterns, and evolutionary trends
.
Zoology
.
1994
;
98
:
165
78
.
8.
Huber
R
,
Van Staaden
MJ
,
Kaufman
LS
,
Liem
KF
.
Microhabitat use, trophic patterns, and the evolution of brain structure in african cichlids
.
Brain Behav Evol
.
1997
;
50
(
3
):
167
82
.
9.
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
.
10.
White
GE
,
Brown
C
.
Microhabitat use affects brain size and structure in intertidal gobies
.
Brain Behav Evol
.
2015
;
85
(
2
):
107
16
.
11.
Wagner
H-J
.
Sensory brain areas in mesopelagic fishes
.
Brain Behav Evol
.
2001
;
57
(
3
):
117
33
.
12.
Schumacher
EL
,
Carlson
BA
.
Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes
.
Elife
.
2002
;
11
:
e74159
.
13.
Lisney
TJ
,
Collin
SP
.
Brain morphology in large pelagic fishes: a comparison between sharks and teleosts
.
J Fish Biol
.
2006
;
68
(
2
):
532
54
.
14.
Yopak
KE
,
Lisney
TJ
,
Collin
SP
,
Montgomery
JC
.
Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans
.
Brain Behav Evol
.
2007
;
69
(
4
):
280
300
.
15.
Gebhardt
IC
,
Hofmann
MH
.
The diversity of the brains of ray-finned fishes
.
Brain Behav Evol
.
2023
;
98
(
4
):
171
82
.
16.
Fong
S
,
Rogell
B
,
Amcoff
M
,
Kotrschal
A
,
van der Bijl
W
,
Buechel
SD
, et al
.
Rapid mosaic brain evolution under artificial selection for relative telencephalon size in the guppy (Poecilia reticulata)
.
Sci Adv
.
2021
;
7
(
46
):
eabj4314
.
17.
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
.
18.
Kolm
N
,
Gonzalez-Voyer
A
,
Brelin
D
,
Winberg
S
.
Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)
.
J Evol Biol
.
2009
;
22
(
12
):
2524
31
.
19.
Kotrschal
A
,
Szorkovszky
A
,
Herbert-Read
J
,
Bloch
NI
,
Romenskyy
M
,
Buechel
SD
, et al
.
Rapid evolution of coordinated and collective movement in response to artificial selection
.
Sci Adv
.
2020
;
6
(
49
):
eaba3148
.
20.
Kotrschal
A
,
Zeng
H-L
,
van der Bijl
W
,
Öhman-Mägi
C
,
Kotrschal
K
,
Pelckmans
K
, et al
.
Evolution of brain region volumes during artificial selection for relative brain size
.
Evolution
.
2017
;
71
(
12
):
2942
51
.
21.
Park
PJ
,
Bell
MA
.
Variation of telencephalon morphology of the threespine stickleback (Gasterosteus aculeatus) in relation to inferred ecology
.
J Evol Biol
.
2010
;
23
(
6
):
1261
77
.
22.
Gonda
A
,
Herczeg
G
,
Merilä
J
.
Adaptive brain size divergence in nine-spined sticklebacks ( Pungitius pungitius )
.
J Evol Biol
.
2009
;
22
(
8
):
1721
6
.
23.
Eifert
C
,
Farnworth
M
,
Schulz-Mirbach
T
,
Riesch
R
,
Bierbach
D
,
Klaus
S
, et al
.
Brain size variation in extremophile fish: local adaptation versus phenotypic plasticity
.
J Zool
.
2015
;
295
(
2
):
143
53
.
24.
Pravosudov
VV
,
Clayton
NS
.
A test of the adaptive specialization hypothesis: population differences in caching, memory, and the Hippocampus in black-capped chickadees (poecile atricapilla)
.
Behav Neurosci
.
2002
;
116
(
4
):
515
22
.
25.
Triki
Z
,
Emery
Y
,
Teles
MC
,
Oliveira
RF
,
Bshary
R
.
Brain morphology predicts social intelligence in wild cleaner fish
.
Nat Commun
.
2020
;
11
(
1
):
6423
.
26.
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
.
27.
Colin
PL
.
Fishes as living tracers of connectivity in the tropical western North Atlantic: I. Distribution of the neon gobies, genus Elacatinus (Pisces: gobiidae)
.
Zootaxa
.
2010
;
2370
(
1
):
36
52
.
28.
Ruber
L
,
Van
TJL
,
Zardoya
R
.
Rapid speciation and ecological divergence in the American seven-spined gobies (gobiidae, gobiosomatini) inferred from a molecular phylogeny
.
Evolution
.
2003
;
57
(
7
):
1584
98
.
29.
Taylor
MS
,
Hellberg
ME
.
Comparative phylogeography in a genus of coral reef fishes: biogeographic and genetic concordance in the Caribbean
.
Mol Ecol
.
2006
;
15
(
3
):
695
707
.
30.
Côté
I
,
Soares
M
.
Gobies as cleaners
. In:
Kapoor
B
, editor.
The biology of gobies
.
Science Publishers
;
2011
[cited 2018 Apr 14]. p.
532
57
. Available from: https://www.crcnetbase.com/doi/10.1201/b11397-28
31.
Colin
PL
.
The neon gobies: comparative biology of the gobies of the genus Gobiosoma
. In:
Subgenus Elacatinus, (pisces: gobiidae) in the tropical western atlantic
.
New Jersey
:
T.F.H. Publications, Neptune
;
1975
.
32.
Whiteman
EA
,
Côté
IM
.
Individual differences in microhabitat use in a Caribbean cleaning goby: a buffer effect in a marine species
.
J Anim Ecol
.
2004
;
73
(
5
):
831
40
.
33.
Whiteman
EA
,
Côté
IM
.
Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons
.
J Fish Biol
.
2002
;
60
(
6
):
1443
58
.
34.
Whiteman
EA
,
Côté
IM
.
Dominance hierarchies in group-living cleaning gobies: causes and foraging consequences
.
Anim Behav
.
2004
;
67
(
2
):
239
47
.
35.
White
JW
,
Grigsby
CJ
,
Warner
RR
.
Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish
.
Coral Reefs
.
2007
;
26
(
1
):
87
94
.
36.
Mazzei
R
,
Lampe
M
,
Ohnesorge
A
,
Pajot
A
,
Soares
MC
,
Bshary
R
.
Ecological differences in the facultative Caribbean cleaning goby Elacatinus prochilos do not predict learning performance in discriminatory two-choice tasks
.
Anim Cogn
.
2019
;
22
(
6
):
1039
50
.
37.
Mazzei
R
,
Soares
MC
,
Bshary
R
.
Social organization variation and behavioural flexibility in the facultative cleaning goby Elacatinus prochilos
.
Anim Behav
.
2021
;
174
:
187
95
.
38.
Thresher
RE
.
Reproduction in reef fishes
.
Neptune City, New Jersey
,
U.S.A.: T.F.H. Publications
;
1984
.
39.
Soares
MC
,
Bshary
R
,
Cardoso
SC
,
Côté
IM
,
Oliveira
RF
.
Face your fears: cleaning gobies inspect predators despite being stressed by them
.
PLoS One
.
2012
;
7
(
6
):
e39781
.
40.
R Core Team
.
R: a language and environment for statistical computing
;
2021
. Available from: https://www.R-project.org/
41.
Mazzei
R
,
Emery
Y
,
Soares
MC
,
Bshary
R
.
Dominance is associated with reduced cleaning activity in group-living Elacatinus prochilos gobies
.
Anim Behav
.
2023
;
206
:
29
38
.
42.
Dunkley
K
,
Ward
AJW
,
Perkins
SE
,
Cable
J
.
To clean or not to clean: cleaning mutualism breakdown in a tidal environment
.
Ecol Evol
.
2020
;
10
(
6
):
3043
54
.
43.
Soares
MC
,
Mazzei
R
,
Cardoso
SC
,
Ramos
C
,
Bshary
R
.
Testosterone causes pleiotropic effects on cleanerfish behaviour
.
Sci Rep
.
2019
;
9
(
1
):
15829
.
44.
Mazzei
R
,
Mendes
TC
,
Cordeiro
CAMM
,
Luque
JL
,
Soares
MC
,
Ferreira
CEL
.
Diet and abundance of the barber goby Elacatinus figaro on Brazilian marginal reefs: ecological predictors and reliance on cleaning interactions
.
Mar Biol
.
2021
;
168
(
5
):
64
.
45.
Butler
AB
,
Hodos
W
.
Comparative vertebrate neuroanatomy: evolution and adaptation
.
John Wiley & Sons
;
2005
[cited 2019 Feb 25]. Available from: https://books.google.com/books/about/Comparative_Vertebrate_Neuroanatomy.html?id=6kGARvykJKMC
46.
Keagy
J
,
Braithwaite
VA
,
Boughman
JW
;
Handling editor: Rudiger Riesch
.
Brain differences in ecologically differentiated sticklebacks
.
Curr Zool
.
2018
;
64
(
2
):
243
50
.
47.
Hofmann
MH
,
Gebhardt
IC
.
Evolution of the visual system in ray-finned fishes
.
Vis Neurosci
.
2023
;
40
:
E005
.
48.
Meek
J
,
Nieuwenhuys
R
.
Holosteans and teleosts
. In:
The central nervous system of vertebrates
;
1998
; p.
759
937
.
49.
Wulliman
M
,
Rupp
B
,
Reichert
H
.
Neuroanatomy of the zebrafish brain: a topological atlas
.
Birkhäuser
;
1996
.
50.
Hagio
H
,
Sato
M
,
Yamamoto
N
.
An ascending visual pathway to the dorsal telencephalon through the optic tectum and nucleus prethalamicus in the yellowfin goby Acanthogobius flavimanus (Temminck & Schlegel, 1845)
.
J Comp Neurol
.
2018
;
526
(
10
):
1733
46
.
51.
Kawaguchi
M
,
Hagio
H
,
Yamamoto
N
,
Matsumoto
K
,
Nakayama
K
,
Akazome
Y
, et al
.
Atlas of the telencephalon based on cytoarchitecture, neurochemical markers, and gene expressions in Rhinogobius flumineus [Mizuno, 1960]
.
J Comp Neurol
.
2019
;
527
(
4
):
874
900
.
52.
Jiang
K
,
Wei
K
,
Chen
SX
,
Huang
J
.
Cytoarchitecture of mudskipper (boleophthalmus pectinirostris) brain
.
Brain Behav Evol
.
2023
;
98
(
3
):
124
47
.
53.
Park
PJ
,
Chase
I
,
Bell
MA
.
Phenotypic plasticity of the threespine stickleback Gasterosteus aculeatus telencephalon in response to experience in captivity
.
Curr Zool
.
2012
;
58
(
1
):
189
210
.
54.
Samuk
K
,
Iritani
D
,
Schluter
D
.
Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks
.
Ecol Evol
.
2014
;
4
(
16
):
3236
43
.
55.
Marchetti
MP
,
Nevitt
GA
.
Effects of hatchery rearing on brain structures of rainbow trout, Oncorhynchus mykiss
.
Environ Biol Fishes
.
2003
;
66
(
1
):
9
14
.
56.
Näslund
J
,
Aarestrup
K
,
Thomassen
ST
,
Johnsson
J
.
Early enrichment effects on brain development in hatchery-reared Atlantic salmon (Salmo salar): no evidence for a critical period
.
Can J Fish Aquat Sci
.
2012
;
69
(
9
):
1481
90
.
57.
McCallum
ES
,
Capelle
PM
,
Balshine
S
.
Seasonal plasticity in telencephalon mass of a benthic fish: seasonal plasticity in telencephalon mass
.
J Fish Biol
.
2014
;
85
(
5
):
1785
92
.
58.
Gonzalez-Voyer
A
,
Winberg
S
,
Kolm
N
.
Social fishes and single mothers: brain evolution in African cichlids
.
Proc Biol Sci
.
2009
;
276
(
1654
):
161
7
.
59.
Costa
SS
,
Andrade
R
,
Carneiro
LA
,
Gonçalves
EJ
,
Kotrschal
K
,
Oliveira
RF
.
Sex differences in the dorsolateral telencephalon correlate with home range size in blenniid fish
.
Brain Behav Evol
.
2011
;
77
(
1
):
55
64
.
60.
Kotrschal
A
,
Räsänen
K
,
Kristjánsson
BK
,
Senn
M
,
Kolm
N
.
Extreme sexual brain size dimorphism in sticklebacks: a consequence of the cognitive challenges of sex and parenting
.
PLoS One
.
2012
;
7
(
1
):
e30055
.
61.
Herczeg
G
,
Välimäki
K
,
Gonda
A
,
Merilä
J
.
Evidence for sex-specific selection in brain: a case study of the nine-spined stickleback
.
J Evol Biol
.
2014
;
27
(
8
):
1604
12
.
62.
Tornabene
L
,
Ahmadia
GN
,
Berumen
ML
,
Smith
DJ
,
Jompa
J
,
Pezold
F
.
Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: gobiidae: Eviota)
.
Mol Phylogenet Evol
.
2013
;
66
(
1
):
391
400
.
63.
Axelrod
CJ
,
Robinson
BW
,
Laberge
F
.
Evolutionary divergence in phenotypic plasticity shapes brain size variation between coexisting sunfish ecotypes
.
J Evol Biol
.
2022
;
35
(
10
):
1363
77
.
You do not currently have access to this content.