Background: The origin and maintenance of species is a unifying theme in evolutionary biology. Mate choice and selection on sexual signals have emerged as powerful drivers of reproductive isolation – the key pillar of the biological species concept. The mechanistic underpinnings of isolating behaviors lie in the circuit- and cellular-level properties of the brain and remain relatively understudied. Summary: Here, I argue that temporal auditory selectivity in anuran amphibians offers a window into the proximate mechanisms of reproductive isolation. First, I discuss anuran behaviors as a longstanding neuroethological model with which to examine behavioral reproductive isolation and its neural correlates. Next, I review how modern neurobiological techniques are revealing the proximate mechanisms of the evolution of divergent mate preferences in anurans, highlighting cellular-level neural shifts in temporal coding. Finally, I discuss future research directions to reveal the neural mechanisms through which behavioral isolation is generated and maintained in anuran model systems. Key Messages: Anurans offer a powerful model for addressing questions about how neural barriers to gene flow arise across biological scales and how changes in the brain contribute to speciation. Modern evolutionary neurobiology will benefit from applying new tools to this longstanding neuroethological model clade.

1.
Hardy
NB
,
Kaczvinsky
C
,
Bird
G
,
Richter
R
,
Dettman
JR
,
Maw
E
, et al
.
Geographic isolation drives speciation in Nearctic aphids
.
Commun Biol
.
2022
;
5
(
1
):
796
.
2.
Dai
X
,
Li
X
,
Huang
Y
,
Liu
X
.
The speciation and adaptation of the polyploids: a case study of the Chinese Isoetes L. diploid-polyploid complex
.
BMC Evol Biol
.
2020
;
20
(
1
):
118
.
3.
Uy
JAC
,
Irwin
DE
,
Webster
MS
.
Behavioral isolation and incipient speciation in birds
.
Annu Rev Ecol Evol Syst
.
2018
;
49
(
1
):
1
24
.
4.
Jang
Y
,
Gerhardt
HC
.
Divergence in female calling song discrimination between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni (Orthoptera: gryllidae)
.
Behav Ecol Sociobiol
.
2006
;
60
(
2
):
150
8
.
5.
Grace
JL
,
Shaw
KL
.
Incipient sexual isolation in Laupala cerasina: females discriminate population-level divergence in acoustic characters
.
Curr Zool
.
2012
;
58
(
3
):
416
25
.
6.
González-Rojas
MF
,
Darragh
K
,
Robles
J
,
Linares
M
,
Schulz
S
,
McMillan
WO
, et al
.
Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies
.
Proc R Soc A B
.
2020
;
287
(
1926
):
20200587
.
7.
Boughman
JW
.
Divergent sexual selection enhances reproductive isolation in sticklebacks
.
Nature
.
2001
;
411
(
6840
):
944
8
.
8.
Gabor
CR
,
Ryan
MJ
.
Geographical variation in reproductive character displacement in mate choice by male sailfin mollies
.
Proc Biol Sci
.
2001
;
268
(
1471
):
1063
70
.
9.
Seehausen
O
,
Terai
Y
,
Magalhaes
IS
,
Carleton
KL
,
Mrosso
HDJ
,
Miyagi
R
, et al
.
Speciation through sensory drive in cichlid fish
.
Nature
.
2008
;
455
(
7213
):
620
6
.
10.
Hoskin
CJ
,
Higgie
M
,
McDonald
KR
,
Moritz
C
.
Reinforcement drives rapid allopatric speciation
.
Nature
.
2005
;
437
(
7063
):
1353
6
.
11.
Lemmon
EM
.
Diversification of conspecific signals in sympatry: geographic overlap drives multidimensional reproductive character displacement in frogs
.
Evolution
.
2009
;
63
(
5
):
1155
70
.
12.
Smadja
C
,
Ganem
G
.
Asymmetrical reproductive character displacement in the house mouse
.
J Evol Biol
.
2005
;
18
(
6
):
1485
93
.
13.
Schuchmann
M
,
Siemers
BM
.
Behavioral evidence for community-wide species discrimination from echolocation calls in bats
.
Am Nat
.
2010
;
176
(
1
):
72
82
.
14.
Baker
MC
,
Baker
AEM
.
Reproductive behavior of female buntings: isolating mechanisms in a hybridizing pair of species
.
Evolution
.
1990
;
44
(
2
):
332
8
.
15.
Kirschel
ANG
,
Blumstein
DT
,
Smith
TB
.
Character displacement of song and morphology in African tinkerbirds
.
Proc Natl Acad Sci USA
.
2009
;
106
(
20
):
8256
61
.
16.
Turbek
SP
,
Browne
M
,
Di Giacomo
AS
,
Kopuchian
C
,
Hochachka
WM
,
Estalles
C
, et al
.
Rapid speciation via the evolution of pre-mating isolation in the Iberá Seedeater
.
Science
.
2021
;
371
(
6536
):
eabc0256
.
17.
Chen
Z
,
Wiens
JJ
.
The origins of acoustic communication in vertebrates
.
Nat Commun
.
2020
;
11
(
1
):
369
.
18.
Gerhardt
HC
,
Bee
MA
.
Recognition and localization of acoustic signals
. In:
Narins
PM
,
Feng
AS
,
Fay
RR
,
Popper
AN
, editors.
Hearing and sound communication in amphibians
.
New York
:
Springer
;
2007
. p.
113
46
.
19.
Sayigh
L
,
Quick
N
,
Hastie
G
,
Tyack
P
.
Repeated call types in short-finned pilot whales, Globicephala macrorhynchus
.
Mar Mamm Sci
.
2013
;
29
(
2
):
312
24
.
20.
Root-Gutteridge
H
,
Bencsik
M
,
Chebli
M
,
Gentle
LK
,
Terrell-Nield
C
,
Bourit
A
, et al
.
Identifying individual wild Eastern grey wolves (Canis lupus lycaon) using fundamental frequency and amplitude of howls
.
Bioacoustics
.
2014
;
23
(
1
):
55
66
.
21.
Weber
T
,
Thorson
J
.
Phonotactic behavior of walking crickets
. In:
Huber
F
,
Moore
TE
,
Loher
W
, editors.
Cricket behavior and neurobiology
.
New York
:
Cornell University Press
;
1989
. p.
310
39
.
22.
Bush
SL
,
Schul
J
.
Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons
.
J Comp Physiol
.
2006
;
192
(
2
):
113
21
.
23.
Kostarakos
K
,
Hedwig
B
.
Pattern recognition in field crickets: concepts and neural evidence
.
J Comp Physiol
.
2015
;
201
(
1
):
73
85
.
24.
Doherty
JA
.
Trade-off phenomena in calling song recognition and phonotaxis in the cricket, Gryllus bimaculatus (Orthoptera, Gryllidae)
.
J Comp Physiol
.
1985
;
156
(
6
):
787
801
.
25.
Hedwig
B
.
Pulses, patterns and paths: neurobiology of acoustic behaviour in crickets
.
J Comp Physiol
.
2006
;
192
(
7
):
677
89
.
26.
Hedwig
BG
.
Sequential filtering processes shape feature detection in crickets: a framework for song pattern recognition
.
Front Physiol
.
2016
;
7
:
46
.
27.
Ohashi
TS
,
Ishikawa
Y
,
Awasaki
T
,
Su
MP
,
Yoneyama
Y
,
Morimoto
N
, et al
.
Evolutionary conservation and diversification of auditory neural circuits that process courtship songs in Drosophila
.
Sci Rep
.
2023
;
13
(
1
):
383
.
28.
Baker
CA
,
Clemens
J
,
Murthy
M
.
Acoustic pattern recognition and courtship songs: insights from insects
.
Annu Rev Neurosci
.
2019
;
42
(
1
):
129
47
.
29.
Rosenthal
GG
,
Rand
AS
,
Ryan
MJ
.
The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback
.
Anim Behav
.
2004
;
68
(
1
):
55
8
.
30.
Starnberger
I
,
Preininger
D
,
Hödl
W
.
From uni- to multimodality: towards an integrative view on anuran communication
.
J Comp Physiol A
.
2014
;
200
(
9
):
777
87
.
31.
Wells
KD
.
The social behaviour of anuran amphibians
.
Anim Behav
.
1977
;
25
:
666
93
.
32.
Gonzalez-Voyer
A
,
den Tex
RJ
,
Castelló
A
,
Leonard
JA
.
Evolution of acoustic and visual signals in Asian barbets
.
J Evol Biol
.
2013
;
26
(
3
):
647
59
.
33.
Johansson
BG
,
Jones
TM
.
The role of chemical communication in mate choice
.
Biol Rev
.
2007
;
82
(
2
):
265
89
.
34.
Gerhardt
HC
,
Huber
F
.
Acoustic communication in insects and anurans: common problems and diverse solutions
.
Chicago
:
University of Chicago Press
;
2002
.
35.
Gerhardt
HC
.
The evolution of vocalization in frogs and toads
.
Annu Rev Ecol Syst
.
1994
;
25
(
1
):
293
324
.
36.
Lemmon
EM
,
Lemmon
AR
.
Reinforcement in chorus frogs: lifetime fitness estimates including intrinsic natural selection and sexual selection against hybrids
.
Evolution
.
2010
;
64
(
6
):
1748
61
.
37.
Gerhardt
HC
.
Geographic variation in acoustic communication: reproductive character displacement and speciation
.
Evol Ecol Res
.
2013
;
15
:
605
32
.
38.
Rose
GJ
,
Gooler
DM
.
Function of the amphibian central auditory system
. In:
Narins
PM
,
Feng
AS
,
Fay
RR
,
Popper
AN
, editors.
Hearing and sound communication in amphibians
.
New York
:
Springer
;
2007
. p.
250
83
.
39.
Feng
A
,
Hall
J
,
Gooler
D
.
Neural basis of sound pattern recognition in anurans
.
Prog Neurobiol
.
1990
;
34
(
4
):
313
29
.
40.
Hall
JC
,
Feng
AS
.
Evidence for parallel processing in the frog’s auditory thalamus
.
J Comp Neurol
.
1987
;
258
(
3
):
407
19
.
41.
Burmeister
SS
.
Neurobiology of female mate choice in frogs: auditory filtering and valuation
.
Integr Comp Biol
.
2017
;
57
(
4
):
857
64
.
42.
Alder
TB
,
Rose
GJ
.
Integration and recovery processes contribute to the temporal selectivity of neurons in the midbrain of the northern leopard frog, Rana pipiens
.
J Comp Physiol
.
2000
;
186
(
10
):
923
37
.
43.
Edwards
CJ
,
Leary
CJ
,
Rose
GJ
.
Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity
.
J Neurophysiol
.
2008
;
100
(
6
):
3407
16
.
44.
Edwards
CJ
,
Alder
TB
,
Rose
GJ
.
Auditory midbrain neurons that count
.
Nat Neurosci
.
2002
;
5
(
10
):
934
6
.
45.
Alder
TB
,
Rose
GJ
.
Long-term temporal integration in the anuran auditory system
.
Nat Neurosci
.
1998
;
1
(
6
):
519
23
.
46.
Littlejohn
MJ
.
Premating isolation in the Hyla ewingi complex (Anura: hylidae)
.
Evolution
.
1965
;
19
(
2
):
234
43
.
47.
Ryan
MJ
,
Perrill
SA
,
Wilczynski
W
.
Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans
.
Am Nat
.
1992
;
139
(
6
):
1370
83
.
48.
Capranica
RR
.
The evoked vocal responses of the bullfrog: a study of communication by sound
.
Cambridge
:
MIT Press
;
1965
.
49.
Straughan
IR
.
An Analysis of the mechanisms of mating call discrimination in the frogs Hyla regilla and
.
Copeia
.
1975
;
1975
(
3
):
415
24
.
50.
Keller
MJ
,
Carl Gerhardt
H
.
Polyploidy alters advertisement call structure in gray treefrogs
.
Proc Biol Sci
.
2001
;
268
(
1465
):
341
5
.
51.
Gerhardt
HC
.
Mating call recognition in the green treefrog (Hyla cinerea): the significance of some fine-scale temporal properties
.
J Exp Biol
.
1978
;
74
(
1
):
59
73
.
52.
Rose
GJ
,
Brenowitz
EA
.
Plasticity of aggressive thresholds in Hyla regilla discrete accommodation to encounter calls
.
Anim Behav
.
1997
;
53
(
2
):
353
61
.
53.
Penna
M
,
Solís
R
,
Moreno-Gómez
FN
.
Diverse patterns of responsiveness to fine temporal features of acoustic signals in a temperate austral forest frog, Batrachyla leptopus (Batrachylidae)
.
Bioacoustics
.
2022
;
31
(
2
):
219
39
.
54.
Davis
MS
.
Acoustically mediated neighbor recognition in the North American bullfrog, Rana catesbeiana
.
Behav Ecol Sociobiol
.
1987
;
21
(
3
):
185
90
.
55.
Bee
MA
,
Gerhardt
HC
.
Neighbour–stranger discrimination by territorial male bullfrogs (Rana catesbeiana): I. Acoustic basis
.
Anim Behav
.
2001
;
62
(
6
):
1129
40
.
56.
Bee
MA
,
Gerhardt
HC
.
Neighbour–stranger discrimination by territorial male bullfrogs (Rana catesbeiana): II. Perceptual basis
.
Anim Behav
.
2001
;
62
(
6
):
1141
50
.
57.
Arak
A
.
Vocal interactions, call matching and territoriality in a Sri Lankan treefrog, Philautus leucorhinus (Rhacophoridae)
.
Anim Behav
.
1983
;
31
(
1
):
292
302
.
58.
Goutte
S
,
Kime
NM
,
Argo IV
TF
,
Ryan
MJ
.
Calling strategies of male túngara frogs in response to dynamic playback
.
Behav
.
2010
;
147
(
1
):
65
83
.
59.
Gerhardt
HC
,
Tanner
SD
,
Corrigan
CM
,
Walton
HC
.
Female preference functions based on call duration in the gray tree frog (Hyla versicolor)
.
Behav Ecol
.
2000
;
11
(
6
):
663
9
.
60.
Blair
WF
.
Mating call in the speciation of anuran amphibians
.
Am Nat
.
1958
;
92
(
862
):
27
51
.
61.
Blair
WF
.
Isolating mechanisms and interspecies interactions in anuran amphibians
.
Q Rev Biol
.
1964
;
39
(
4
):
334
44
.
62.
Blair
WF
.
Character displacement in frogs
.
Am Zool
.
1974
;
14
(
4
):
1119
25
.
63.
Littlejohn
MJ
,
Loftus-Hills
JJ
.
An experimental evaluation of premating isolation in the Hyla ewingi complex (Anura: hylidae)
.
Evolution
.
1968
;
22
(
4
):
659
63
.
64.
Capranica
RR
,
Frishkopf
LS
,
Nevo
E
.
Encoding of geographic dialects in the auditory system of the cricket frog
.
Science
.
1973
;
182
(
4118
):
1272
5
.
65.
Simmons
AM
.
“To Ear is Human, to Frogive is Divine”: bob Capranica’s legacy to auditory neuroethology
.
J Comp Physiol A
.
2013
;
199
(
3
):
169
82
.
66.
Capranica
RR
,
Moffat
AJM
.
Neurobehavioral correlates of sound communication in anurans
. In:
Ewert
JP
,
Capranica
RR
,
Ingle
D
, eds.
Advances in vertebrate neuroethology
.
New York
:
Plenum Press
;
1983
. p.
701
30
.
67.
Hillery
CM
,
Narins
PM
.
Frequency and time domain comparison of low frequency auditory fiber responses in two anuran amphibians
.
Hear Res
.
1987
;
25
(
2–3
):
233
48
.
68.
Narins
PM
,
Wagner
I
.
Noise susceptibility and immunity of phase locking in amphibian auditory-nerve fibers
.
J Acoust Soc Am
.
1989
;
85
(
3
):
1255
65
.
69.
Megela
AL
,
Capranica
RR
.
Response patterns to tone bursts in peripheral auditory system of anurans
.
J Neurophysiol
.
1981
;
46
(
3
):
465
78
.
70.
Rose
G
,
Capranica
RR
.
Temporal selectivity in the central auditory system of the leopard frog
.
Science
.
1983
;
219
(
4588
):
1087
9
.
71.
Matesz
C
.
Central projection of the VIIIth cranial nerve in the frog
.
Neuroscience
.
1979
;
4
(
12
):
2061
71
.
72.
Fuzessery
ZM
,
Feng
AS
.
Frequency selectivity in the anuran auditory midbrain: single unit responses to single and multiple tone stimulation
.
J Comp Physiol
.
1982
;
146
(
4
):
471
84
.
73.
Feng
A
.
Afferent and efferent innervation patterns of the cochlear nucleus (dorsal medullary nucleus) of the leopard frog
.
Brain Res
.
1986
;
367
(
1–2
):
183
91
.
74.
Rose
GJ
,
Capranica
RR
.
Sensitivity to amplitude modulated sounds in the anuran auditory nervous system
.
J Neurophysiol
.
1985
;
53
(
2
):
446
65
.
75.
Hall
JC
,
Feng
AS
.
Classification of the temporal discharge patterns of single auditory neurons in the dorsal medullary nucleus of the northern leopard frog
.
J Neurophysiol
.
1990
;
64
(
5
):
1460
73
.
76.
Hall
JC
,
Feng
AS
.
Temporal processing in the dorsal medullary nucleus of the Northern leopard frog (Rana pipiens pipiens)
.
J Neurophysiol
.
1991
;
66
(
3
):
955
73
.
77.
Hall
JC
,
Feng
AS
.
Influence of envelope rise time on neural responses in the auditory system of anurans
.
Hear Res
.
1988
;
36
(
2–3
):
261
76
.
78.
Condon
CJ
,
Chang
S-H
,
Feng
AS
.
Processing of behaviorally relevant temporal parameters of acoustic stimuli by single neurons in the superior olivary nucleus of the leopard frog
.
J Comp Physiol
.
1991
;
168
(
6
):
709
25
.
79.
Condon
CJ
,
Chang
S-H
,
Feng
AS
.
Classification of the temporal discharge patterns of single auditory neurons in the frog superior olivary nucleus
.
Hear Res
.
1995
;
83
(
1–2
):
190
202
.
80.
Rose
GJ
,
Capranica
RR
.
Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters
.
J Comp Physiol
.
1984
;
154
(
2
):
211
9
.
81.
Rose
GJ
,
Hanson
JL
,
Leary
CJ
,
Graham
JA
,
Alluri
RK
,
Vasquez-Opazo
GA
.
Species-specificity of temporal processing in the auditory midbrain of gray treefrogs: interval-counting neurons
.
J Comp Physiol
.
2015
;
201
(
5
):
485
503
.
82.
Simmons
AM
,
Sanderson
MI
,
Garabedian
CE
.
Representation of waveform periodicity in the auditory midbrain of the bullfrog, Rana catesbeiana
.
JARO
.
2000
;
1
(
1
):
2
24
.
83.
Wilczynski
W
,
Endepols
H
.
Central auditory pathways in anuran amphibians: the anatomical basis of hearing and sound communication
. In:
Narins
PM
,
Feng
AS
,
Fay
RR
,
Popper
AN
, editors.
Hearing and sound communication in amphibians
.
New York
:
Springer
;
2007
. p.
221
49
.
84.
Hoke
KL
,
Burmeister
SS
,
Fernald
RD
,
Rand
AS
,
Ryan
MJ
,
Wilczynski
W
.
Functional mapping of the auditory midbrain during mate call reception
.
J Neurosci
.
2004
;
24
(
50
):
11264
72
.
85.
Moreno
N
,
González
A
.
Central amygdala in anuran amphibians: neurochemical organization and connectivity
.
J Comp Neurol
.
2005
;
489
(
1
):
69
91
.
86.
Hall
IC
,
Ballagh
IH
,
Kelley
DB
.
The Xenopus amygdala mediates socially appropriate vocal communication signals
.
J Neurosci
.
2013
;
33
(
36
):
14534
48
.
87.
Kelley
DB
.
Neuroeffectors for vocalization in Xenopus laevis: hormonal regulation of sexual dimorphism
.
J Neurobiol
.
1986
;
17
(
3
):
231
48
.
88.
Wetzel
DM
,
Haerter
UL
,
Kelley
DB
.
A proposed neural pathway for vocalization in South African clawed frogs, Xenopus laevis
.
J Comp Physiol
.
1985
;
157
(
6
):
749
61
.
89.
Swanson
LW
.
Cerebral hemisphere regulation of motivated behavior11Published on the world wide web on 2 november 2000
.
Brain Res
.
2000
;
886
(
1–2
):
113
64
.
90.
Martínez-García
F
,
Novejarque
A
,
Lanuza
E
.
Two interconnected functional systems in the amygdala of amniote vertebrates
.
Brain Res Bull
.
2008
;
75
(
2–4
):
206
13
.
91.
Abellán
A
,
Medina
L
.
Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development
.
J Comp Neurol
.
2009
;
515
(
4
):
465
501
.
92.
Schmidt
RS
.
Mating call phonotaxis in female American toads: lesions of central auditory system
.
Brain Behav Evol
.
1988
;
32
(
2
):
119
28
.
93.
Endepols
H
,
Feng
AS
,
Gerhardt
HC
,
Schul
J
,
Walkowiak
W
.
Roles of the auditory midbrain and thalamus in selective phonotaxis in female gray treefrogs (Hyla versicolor)
.
Behav Brain Res
.
2003
;
145
(
1–2
):
63
77
.
94.
Hoke
KL
,
Ryan
MJ
,
Wilczynski
W
.
Integration of sensory and motor processing underlying social behaviour in túngara frogs
.
Proc Biol Sci
.
2007
;
274
(
1610
):
641
9
.
95.
Chakraborty
M
,
Mangiamele
LA
,
Burmeister
SS
.
Neural activity patterns in response to interspecific and intraspecific variation in mating calls in the túngara frog
.
PLoS One
.
2010
;
5
(
9
):
e12898
.
96.
Chakraborty
M
,
Burmeister
SS
.
Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of túngara frogs
.
Horm Behav
.
2010
;
58
(
4
):
619
27
.
97.
Chakraborty
M
,
Burmeister
SS
.
Estradiol induces sexual behavior in female túngara frogs
.
Horm Behav
.
2009
;
55
(
1
):
106
12
.
98.
Chakraborty
M
,
Burmeister
SS
.
Effects of estradiol on neural responses to social signals in female túngara frogs
.
J Exp Biol
.
2015
;
218
(
Pt 22
):
3671
7
.
99.
Diekamp
B
,
Schneider
H
.
Neuronal processing of conspecific and related calls in the torus semicircularis of Rana r. ridibunda Pall. (Anura): single-unit recordings
.
J Comp Physiol
.
1988
;
163
(
3
):
301
15
.
100.
Elliott
TM
,
Christensen-Dalsgaard
J
,
Kelley
DB
.
Temporally selective processing of communication signals by auditory midbrain neurons
.
J Neurophysiol
.
2011
;
105
(
4
):
1620
32
.
101.
Rose
GJ
.
The numerical abilities of anurans and their neural correlates: insights from neuroethological studies of acoustic communication
.
Philos Trans R Soc Lond B Biol Sci
.
2017
;
373
(
1740
):
20160512
.
102.
Hanson
JL
,
Rose
GJ
,
Leary
CJ
,
Graham
JA
,
Alluri
RK
,
Vasquez-Opazo
GA
.
Species specificity of temporal processing in the auditory midbrain of gray treefrogs: long-interval neurons
.
J Comp Physiol A
.
2016
;
202
(
1
):
67
79
.
103.
Rose
GJ
.
Time computations in anuran auditory systems
.
Front Physiol
.
2014
;
5
:
206
.
104.
Gupta
S
,
Alluri
RK
,
Rose
GJ
,
Bee
MA
.
Neural basis of acoustic species recognition in a cryptic species complex
.
J Exp Biol
.
2021
;
224
(
23
):
jeb243405
.
105.
Naud
R
,
Houtman
D
,
Rose
GJ
,
Longtin
A
.
Counting on dis-inhibition: a circuit motif for interval counting and selectivity in the anuran auditory system
.
J Neurophysiol
.
2015
;
114
(
5
):
2804
15
.
106.
Alluri
RK
,
Rose
GJ
,
Leary
CJ
,
Palaparthi
A
,
Hanson
JL
,
Vasquez-Opazo
GA
, et al
.
How auditory selectivity for sound timing arises: the diverse roles of GABAergic inhibition in shaping the excitation to interval-selective midbrain neurons
.
Prog Neurobiol
.
2021
;
199
:
101962
.
107.
Bochet
P
,
Audinat
E
,
Lambolez
B
,
Crépel
F
,
Rossier
J
,
Iino
M
, et al
.
Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel
.
Neuron
.
1994
;
12
(
2
):
383
8
.
108.
Angulo
MC
,
Lambolez
B
,
Audinat
E
,
Hestrin
S
,
Rossier
J
.
Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells
.
J Neurosci
.
1997
;
17
(
17
):
6685
96
.
109.
Mayer
M
,
Westbrook
G
,
Guthrie
P
.
Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones
.
Nature
.
1984
;
309
(
5965
):
261
3
.
110.
Gerhardt
HC
.
Acoustic spectral preferences in two cryptic species of grey treefrogs: implications for mate choice and sensory mechanisms
.
Anim Behav
.
2005
;
70
(
1
):
39
48
.
111.
Gerhardt
HC
,
Doherty
JA
.
Acoustic communication in the gray treefrog, Hyla versicolor: evolutionary and neurobiological implications
.
J Comp Physiol
.
1988
;
162
(
2
):
261
78
.
112.
Klump
GM
,
Gerhardt
HC
.
Use of non-arbitrary acoustic criteria in mate choice by female gray tree frogs
.
Nature
.
1987
;
326
(
6110
):
286
8
.
113.
Ward
JL
,
Love
EK
,
Vélez
A
,
Buerkle
NP
,
O’Bryan
LR
,
Bee
MA
.
Multitasking males and multiplicative females: dynamic signalling and receiver preferences in Cope’s grey treefrog
.
Anim Behav
.
2013
;
86
(
2
):
231
43
.
114.
Krishna
BS
,
Semple
MN
.
Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus
.
J Neurophysiol
.
2000
;
84
(
1
):
255
73
.
115.
Pinheiro
AD
,
Wu
M
,
Jen
PH
.
Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus
.
J Comp Physiol
.
1991
;
169
(
1
):
69
85
.
116.
Burger
RM
,
Pollak
GD
.
Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus
.
J Neurophysiol
.
1998
;
80
(
4
):
1686
701
.
117.
Jen
PH-S
,
Wu
CH
.
The role of GABAergic inhibition in shaping the response size and duration selectivity of bat inferior collicular neurons to sound pulses in rapid sequences
.
Hear Res
.
2005
;
202
(
1–2
):
222
34
.
118.
Bass
AH
,
McKibben
JR
.
Neural mechanisms and behaviors for acoustic communication in teleost fish
.
Prog Neurobiol
.
2003
;
69
(
1
):
1
26
.
119.
Araki
M
,
Bandi
MM
,
Yazaki-Sugiyama
Y
.
Mind the gap: neural coding of species identity in birdsong prosody
.
Science
.
2016
;
354
(
6317
):
1282
7
.
120.
Inda
M
,
Hotta
K
,
Oka
K
.
Neural properties of fundamental function encoding of sound selectivity in the female avian auditory cortex
.
Eur J Neurosci
.
2020
;
51
(
8
):
1770
83
.
121.
Carlson
BA
.
Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior
.
J Neurosci
.
2009
;
29
(
30
):
9417
28
.
122.
Yamada
D
,
Ishimoto
H
,
Li
X
,
Kohashi
T
,
Ishikawa
Y
,
Kamikouchi
A
.
GABAergic local interneurons shape female fruit fly response to mating songs
.
J Neurosci
.
2018
;
38
(
18
):
4329
47
.
123.
Diekamp
B
,
Gerhardt
HC
.
Selective phonotaxis to advertisement calls in the gray treefrog Hyla versicolor: behavioral experiments and neurophysiological correlates
.
J Comp Physiol
.
1995
;
177
(
2
):
173
90
.
124.
Gooler
DM
,
Feng
AS
.
Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli
.
J Neurophysiol
.
1992
;
67
(
1
):
1
22
.
125.
Epping
WJM
,
Eggermont
JJ
.
Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. II. Stimulation with amplitude modulated sound
.
Hear Res
.
1986
;
24
(
1
):
55
72
.
126.
Lynch
KS
,
Wilczynski
W
.
Reproductive hormones modify reception of species-typical communication signals in a female anuran
.
Brain Behav Evol
.
2008
;
71
(
2
):
143
50
.
127.
O’Bryant
EL
,
Wilczynski
W
.
Changes in plasma testosterone levels and brain AVT cell number during the breeding season in the green treefrog
.
Brain Behav Evol
.
2010
;
75
(
4
):
271
81
.
128.
Goodson
JL
,
Kabelik
D
.
Dynamic limbic networks and social diversity in vertebrates: from neural context to neuromodulatory patterning
.
Front Neuroendocrinol
.
2009
;
30
(
4
):
429
41
.
129.
DeAngelis
RS
,
Hofmann
HA
.
Neural and molecular mechanisms underlying female mate choice decisions in vertebrates
.
J Exp Biol
.
2020
;
223
(
Pt 17
):
jeb207324
.
130.
Moreno
N
,
González
A
.
Hodological characterization of the medial amygdala in anuran amphibians
.
J Comp Neurol
.
2003
;
466
(
3
):
389
408
.
131.
Barton
RA
,
Harvey
PH
.
Mosaic evolution of brain structure in mammals
.
Nature
.
2000
;
405
(
6790
):
1055
8
.
132.
Finlay
BL
,
Darlington
RB
,
Nicastro
N
.
Developmental structure in brain evolution
.
Behav Brain Sci
.
2001
;
24
(
2
):
263
78
.
133.
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
.
134.
Loomis
C
,
Peuß
R
,
Jaggard
JB
,
Wang
Y
,
McKinney
SA
,
Raftopoulos
SC
, et al
.
An adult brain atlas reveals broad neuroanatomical changes in independently evolved populations of Mexican cavefish
.
Front Neuroanat
.
2019
;
13
:
88
.
135.
York
RA
,
Byrne
A
,
Abdilleh
K
,
Patil
C
,
Streelman
T
,
Finger
TE
, et al
.
Behavioral evolution contributes to hindbrain diversification among Lake Malawi cichlid fish
.
Sci Rep
.
2019
;
9
(
1
):
19994
.
136.
Stöckl
AL
,
Ribi
WA
,
Warrant
EJ
.
Adaptations for nocturnal and diurnal vision in the hawkmoth lamina
.
J Comp Neurol
.
2016
;
524
(
1
):
160
75
.
137.
Keesey
IW
,
Grabe
V
,
Knaden
M
,
Hansson
BS
.
Divergent sensory investment mirrors potential speciation via niche partitioning across Drosophila
.
Elife
.
2020
;
9
:
e57008
.
138.
Montgomery
SH
,
Rossi
M
,
McMillan
WO
,
Merrill
RM
.
Neural divergence and hybrid disruption between ecologically isolated Heliconius butterflies
.
Proc Natl Acad Sci USA
.
2021
;
118
(
6
):
e2015102118
.
139.
Zeng
Y
,
Lou
SL
,
Liao
WB
,
Jehle
R
,
Kotrschal
A
.
Sexual selection impacts brain anatomy in frogs and toads
.
Ecol Evol
.
2016
;
6
(
19
):
7070
9
.
140.
Tripp
JA
,
Feng
NY
,
Bass
AH
.
To hum or not to hum: neural transcriptome signature of male courtship vocalization in a teleost fish
.
Genes Brain Behav
.
2021
;
20
(
6
):
e12740
.
141.
Mobley
RB
,
Ray
EJ
,
Maruska
KP
.
Expression and localization of neuronal nitric oxide synthase in the brain and sensory tissues of the African cichlid fish Astatotilapia burtoni
.
J Comp Neurol
.
2022
;
530
(
16
):
2901
17
.
142.
Vernaz
G
,
Hudson
AG
,
Santos
ME
,
Fischer
B
,
Carruthers
M
,
Shechonge
AH
, et al
.
Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish
.
Nat Ecol Evol
.
2022
;
6
(
12
):
1940
51
.
143.
Lynch
KS
,
Ramsey
ME
,
Cummings
ME
.
The mate choice brain: comparing gene profiles between female choice and male coercive poeciliids
.
Genes Brain Behav
.
2012
;
11
(
2
):
222
9
.
144.
Ramsey
ME
,
Maginnis
TL
,
Wong
RY
,
Brock
C
,
Cummings
ME
.
Identifying context-specific gene profiles of social, reproductive, and mate preference behavior in a fish species with female mate choice
.
Front Neurosci
.
2012
;
6
:
62
.
145.
Bloch
NI
,
Corral-López
A
,
Buechel
SD
,
Kotrschal
A
,
Kolm
N
,
Mank
JE
.
Early neurogenomic response associated with variation in guppy female mate preference
.
Nat Ecol Evol
.
2018
;
2
(
11
):
1772
81
.
146.
Ramsdell
KMM
,
Lyons-Sobaski
SA
,
Robertson
HM
,
Walden
KKO
,
Feder
JL
,
Wanner
K
, et al
.
Expressed sequence tags from cephalic chemosensory organs of the Northern walnut husk fly, Rhagoletis suavis, including a putative canonical odorant receptor
.
J Insect Sci
.
2010
;
10
(
51
):
51
11
.
147.
Ragland
GJ
,
Egan
SP
,
Feder
JL
,
Berlocher
SH
,
Hahn
DA
.
Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella
.
J Exp Biol
.
2011
;
214
(
Pt 23
):
3948
59
.
148.
Catalan
A
,
Macias-Munoz
A
,
Briscoe
AD
.
Evolution of sex-biased gene expression and dosage compensation in the eye and brain of Heliconius butterflies
.
Mol Biol Evol
.
2018
;
35
(
9
):
2120
34
.
149.
Rossi
M
,
Hausmann
AE
,
Thurman
TJ
,
Montgomery
SH
,
Papa
R
,
Jiggins
CD
, et al
.
Visual mate preference evolution during butterfly speciation is linked to neural processing genes
.
Nat Commun
.
2020
;
11
(
1
):
4763
.
150.
Laturney
M
,
Billeter
J-C
.
Neurogenetics of female reproductive behaviors in Drosophila melanogaster
. In:
Friedmann
T
,
Dunlap
JC
,
Goodwin
SF
, editors.
Advances in genetics
.
Elsevier
;
2014
. Vol.
Vol. 85
. p.
1
108
.
151.
Whitfield
CW
,
Cziko
A-M
,
Robinson
GE
.
Gene expression profiles in the brain predict behavior in individual honey bees
.
Science
.
2003
;
302
(
5643
):
296
9
.
152.
Chandrasekaran
S
,
Ament
SA
,
Eddy
JA
,
Rodriguez-Zas
SL
,
Schatz
BR
,
Price
ND
, et al
.
Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states
.
Proc Natl Acad Sci USA
.
2011
;
108
(
44
):
18020
5
.
153.
Zayed
A
,
Robinson
GE
.
Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee
.
Annu Rev Genet
.
2012
;
46
(
1
):
591
615
.
154.
Young
LJ
,
Nilsen
R
,
Waymire
KG
,
MacGregor
GR
,
Insel
TR
.
Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole
.
Nature
.
1999
;
400
(
6746
):
766
8
.
155.
Insel
TR
,
Young
LJ
.
The neurobiology of attachment
.
Nat Rev Neurosci
.
2001
;
2
:
129
36
.
156.
Ospina
OE
,
Lemmon
AR
,
Dye
M
,
Zdyrski
C
,
Holland
S
,
Stribling
D
, et al
.
Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)
.
BMC Genomics
.
2021
;
22
(
1
):
711
.
157.
Knight
ZA
,
Tan
K
,
Birsoy
K
,
Schmidt
S
,
Garrison
JL
,
Wysocki
RW
, et al
.
Molecular profiling of activated neurons by phosphorylated ribosome capture
.
Cell
.
2012
;
151
(
5
):
1126
37
.
158.
Megela-Simmons
A
,
Moss
CF
,
Daniel
KM
.
Behavioral audiograms of the bullfrog (Rana catesbeiana) and the green tree frog (Hyla cinerea)
.
J Acoust Soc Am
.
1985
;
78
(
4
):
1236
44
.
159.
Wilczynski
W
,
Rand
AS
,
Ryan
MJ
.
Evolution of calls and auditory tuning in the Physalaemus pustulosus species group
.
Brain Behav Evol
.
2001
;
58
(
3
):
137
51
.
160.
James
LS
,
Taylor
RC
,
Hunter
KL
,
Ryan
MJ
.
Evolutionary and allometric insights into anuran auditory sensitivity and morphology
.
Brain Behav Evol
.
2022
;
97
(
3–4
):
140
50
.
161.
Ryan
MJ
.
Neuroanatomy influences speciation rates among anurans
.
Proc Natl Acad Sci
.
1986
;
83
(
5
):
1379
82
.
162.
Ryan
MJ
.
Signals, species, and sexual selection
.
Am Sci
.
1990
;
78
(
1
):
46
52
.
163.
Feng
AS
,
Lin
W-Y
.
Neuronal architecture of the dorsal nucleus (Cochlear nucleus) of the frog, Rana pipiens pipiens
.
J Comp Neurol
.
1996
;
366
(
2
):
320
34
.
164.
Walkowiak
W
.
Two auditory filter systems determine the calling behavior of the fire-bellied toad: a behavioral and neurophysiological characterization
.
J Comp Physiol
.
1988
;
164
(
1
):
31
41
.
165.
Hoke
KL
,
Christensen-Dalsgaard
J
,
Womack
MC
.
Peripheral auditory system divergence does not explain species differences in call preference
.
Brain Behav Evol
.
2022
;
97
(
3–4
):
151
66
.
166.
Smallwood
PM
,
Ölveczky
BP
,
Williams
GL
,
Jacobs
GH
,
Reese
BE
,
Meister
M
, et al
.
Genetically engineered mice with an additional class of cone photoreceptors: implications for the evolution of color vision
.
Proc Natl Acad Sci USA
.
2003
;
100
(
20
):
11706
11
.
167.
Jacobs
GH
,
Williams
GA
,
Cahill
H
,
Nathans
J
.
Emergence of novel color vision in mice engineered to express a human cone photopigment
.
Science
.
2007
;
315
(
5819
):
1723
5
.
168.
Mancuso
K
,
Hauswirth
WW
,
Li
Q
,
Connor
TB
,
Kuchenbecker
JA
,
Mauck
MC
, et al
.
Gene therapy for red-green colour blindness in adult primates
.
Nature
.
2009
;
461
(
7265
):
784
7
.
169.
West-Eberhard
MJ
.
Sexual selection, social competition, and speciation
.
Q Rev Biol
.
1983
;
58
(
2
):
155
83
.
170.
Pfennig
DW
,
Wund
MA
,
Snell-Rood
EC
,
Cruickshank
T
,
Schlichting
CD
,
Moczek
AP
.
Phenotypic plasticity’s impacts on diversification and speciation
.
Trends Ecol Evol
.
2010
;
25
(
8
):
459
67
.
171.
Snell-Rood
EC
.
An overview of the evolutionary causes and consequences of behavioural plasticity
.
Anim Behav
.
2013
;
85
(
5
):
1004
11
.
172.
Roth
TC
,
LaDage
LD
,
Freas
CA
,
Pravosudov
VV
.
Variation in memory and the hippocampus across populations from different climates: a common garden approach
.
Proc Biol Sci
.
2012
;
279
(
1727
):
402
10
.
173.
Montgomery
SH
,
Merrill
RM
.
Divergence in brain composition during the early stages of ecological specialization in Heliconius butterflies
.
J Evol Biol
.
2017
;
30
(
3
):
571
82
.
174.
Liu
Y
,
Jones
CD
,
Day
LB
,
Summers
K
,
Burmeister
SS
.
Cognitive phenotype and differential gene expression in a hippocampal homologue in two species of frog
.
Integr Comp Biol
.
2020
;
60
(
4
):
1007
23
.
175.
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
(
1
):
75
.
176.
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
.
177.
Vila-Pouca
C
,
De Waele
H
,
Kotrschal
A
.
The effect of experimental hybridization on cognition and brain anatomy: limited phenotypic variation and transgression in Poeciliidae
.
Evolution
.
2022
;
76
(
12
):
2864
78
.
178.
Jourjine
N
,
Hoekstra
HE
.
Expanding evolutionary neuroscience: insights from comparing variation in behavior
.
Neuron
.
2021
;
109
(
7
):
1084
99
.
You do not currently have access to this content.