Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards

The brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can undergo different selective pressures over the course of evolution, and as selection acts on the outputs of brain function, it necessarily alt...

Full description

Saved in:
Bibliographic Details
Published inBrain, behavior and evolution Vol. 90; no. 3; p. 211
Main Authors Hoops, Daniel, Vidal-García, Marta, Ullmann, Jeremy F P, Janke, Andrew L, Stait-Gardner, Timothy, Duchêne, David A, Price, William S, Whiting, Martin J, Keogh, J Scott
Format Journal Article
LanguageEnglish
Published Switzerland 01.01.2017
Subjects
Online AccessGet more information

Cover

Loading…
Abstract The brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can undergo different selective pressures over the course of evolution, and as selection acts on the outputs of brain function, it necessarily alters the structure of the brain. Two models have been proposed to explain the evolutionary patterns observed in brain morphology. The concerted brain evolution model posits that the brain evolves as a single unit and the evolution of different brain regions are coordinated. The mosaic brain evolution model posits that brain regions evolve independently of each other. It is now understood that both models are responsible for driving changes in brain morphology; however, which factors favour concerted or mosaic brain evolution is unclear. Here, we examined the volumes of the 6 major neural subdivisions across 14 species of the agamid lizard genus Ctenophorus (dragons). These species have diverged multiple times in behaviour, ecology, and body morphology, affording a unique opportunity to test neuroevolutionary models across species. We assigned each species to an ecomorph based on habitat use and refuge type, then used MRI to measure total and regional brain volume. We found evidence for both mosaic and concerted brain evolution in dragons: concerted brain evolution with respect to body size, and mosaic brain evolution with respect to ecomorph. Specifically, all brain subdivisions increase in volume relative to body size, yet the tectum and rhombencephalon also show opposite patterns of evolution with respect to ecomorph. Therefore, we find that both models of evolution are occurring simultaneously in the same structures in dragons, but are only detectable when examining particular drivers of selection. We show that the answer to the question of whether concerted or mosaic brain evolution is detected in a system can depend more on the type of selection measured than on the clade of animals studied.
AbstractList The brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can undergo different selective pressures over the course of evolution, and as selection acts on the outputs of brain function, it necessarily alters the structure of the brain. Two models have been proposed to explain the evolutionary patterns observed in brain morphology. The concerted brain evolution model posits that the brain evolves as a single unit and the evolution of different brain regions are coordinated. The mosaic brain evolution model posits that brain regions evolve independently of each other. It is now understood that both models are responsible for driving changes in brain morphology; however, which factors favour concerted or mosaic brain evolution is unclear. Here, we examined the volumes of the 6 major neural subdivisions across 14 species of the agamid lizard genus Ctenophorus (dragons). These species have diverged multiple times in behaviour, ecology, and body morphology, affording a unique opportunity to test neuroevolutionary models across species. We assigned each species to an ecomorph based on habitat use and refuge type, then used MRI to measure total and regional brain volume. We found evidence for both mosaic and concerted brain evolution in dragons: concerted brain evolution with respect to body size, and mosaic brain evolution with respect to ecomorph. Specifically, all brain subdivisions increase in volume relative to body size, yet the tectum and rhombencephalon also show opposite patterns of evolution with respect to ecomorph. Therefore, we find that both models of evolution are occurring simultaneously in the same structures in dragons, but are only detectable when examining particular drivers of selection. We show that the answer to the question of whether concerted or mosaic brain evolution is detected in a system can depend more on the type of selection measured than on the clade of animals studied.
Author Ullmann, Jeremy F P
Janke, Andrew L
Keogh, J Scott
Stait-Gardner, Timothy
Hoops, Daniel
Price, William S
Duchêne, David A
Vidal-García, Marta
Whiting, Martin J
Author_xml – sequence: 1
  givenname: Daniel
  surname: Hoops
  fullname: Hoops, Daniel
  organization: Division of Ecology and Evolution, Research School of Biology, The Australian National University, Acton, ACT, Australia
– sequence: 2
  givenname: Marta
  surname: Vidal-García
  fullname: Vidal-García, Marta
– sequence: 3
  givenname: Jeremy F P
  surname: Ullmann
  fullname: Ullmann, Jeremy F P
– sequence: 4
  givenname: Andrew L
  surname: Janke
  fullname: Janke, Andrew L
– sequence: 5
  givenname: Timothy
  surname: Stait-Gardner
  fullname: Stait-Gardner, Timothy
– sequence: 6
  givenname: David A
  surname: Duchêne
  fullname: Duchêne, David A
– sequence: 7
  givenname: William S
  surname: Price
  fullname: Price, William S
– sequence: 8
  givenname: Martin J
  surname: Whiting
  fullname: Whiting, Martin J
– sequence: 9
  givenname: J Scott
  surname: Keogh
  fullname: Keogh, J Scott
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28869944$$D View this record in MEDLINE/PubMed
BookMark eNo1j8lKBDEYhIMozqIHX0DyAq1ZO3-O2rYLtHjR85BVIjPJkJ4Z0Ke3RT3VV3xQUAt0nEsOCF1QckWp1NeEEKFAcThCcyoYbbQSfIYW4_jxo5igp2jGAFqthZijrj8kH7ILOJaKuzJR3QWPTfb4uYwmOXxbTcq4P5T1fpdKxlO5q-Z9oiF9merHM3QSzXoM53-5RG_3_Wv32AwvD0_dzdA4LuiuEZ4FRaMi1joHLSHMaQUcbFTMRRNUK722k_FSypYDRGk4pVa14ICYyJbo8nd3u7eb4Ffbmjamfq7-37BvH2ZJ5Q
CitedBy_id crossref_primary_10_7554_eLife_80777
crossref_primary_10_1159_000509069
crossref_primary_10_1002_ece3_5164
crossref_primary_10_1098_rspb_2021_2784
crossref_primary_10_7554_eLife_74159
crossref_primary_10_1093_icb_icaa129
crossref_primary_10_1002_cne_25469
crossref_primary_10_1038_s41597_022_01364_9
crossref_primary_10_1093_icb_icae075
crossref_primary_10_1098_rspb_2018_1971
crossref_primary_10_7554_eLife_68809
crossref_primary_10_1002_ar_25212
crossref_primary_10_1038_s41467_019_13405_w
crossref_primary_10_1016_j_cub_2018_10_038
crossref_primary_10_1159_000509070
crossref_primary_10_1093_biolinnean_bly206
crossref_primary_10_1111_jeb_13763
crossref_primary_10_1186_s12864_020_06908_0
crossref_primary_10_3389_fphys_2021_612865
crossref_primary_10_1002_cne_24480
crossref_primary_10_1016_j_tics_2022_02_003
crossref_primary_10_1186_s12915_021_01024_1
crossref_primary_10_1007_s00429_021_02282_z
crossref_primary_10_1016_j_beproc_2020_104223
crossref_primary_10_1159_000486529
crossref_primary_10_1111_joa_13664
crossref_primary_10_1007_s00429_024_02788_2
crossref_primary_10_1111_jeb_13299
crossref_primary_10_1163_1568539X_bja10104
ContentType Journal Article
Copyright 2017 S. Karger AG, Basel.
Copyright_xml – notice: 2017 S. Karger AG, Basel.
DBID CGR
CUY
CVF
ECM
EIF
NPM
DOI 10.1159/000478738
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
DatabaseTitleList MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Zoology
Ecology
EISSN 1421-9743
ExternalDocumentID 28869944
Genre Journal Article
GroupedDBID ---
--Z
-~X
.GJ
0R~
0~5
0~B
23N
30W
325
36B
3O.
3V.
4.4
53G
5GY
5RE
6J9
7X2
7X7
7XC
88E
88I
8AF
8AO
8CJ
8FE
8FH
8FI
8FJ
8UI
AAYIC
ABIVO
ABJNI
ABPAZ
ABTAH
ABUWG
ACCUC
ACGFO
ACGFS
ACGOD
ACKIV
ACNCT
ACPRK
ACPSR
ADAGL
ADBBV
ADGES
AENEX
AEYAO
AFJJK
AFKRA
AFRAH
AHMBA
AI.
ALDHI
ALIPV
ALMA_UNASSIGNED_HOLDINGS
ATCPS
AZPMC
AZQEC
BBNVY
BCR
BCU
BEC
BENPR
BHPHI
BLC
BPHCQ
BVXVI
CAG
CCPQU
CGR
COF
CS3
CUY
CVF
CYUIP
D1J
D1K
DU5
DWQXO
E0A
EBS
ECM
EIF
EJD
EMB
EMOBN
F5P
FB.
FYUFA
GNUQQ
HCIFZ
HMCUK
HZ~
IY7
K6-
KUZGX
L7B
LK5
LK8
M0K
M1P
M2M
M2P
M7P
M7R
NPM
O1H
O9-
OHT
P2P
PATMY
PEA
PQQKQ
PROAC
PSQYO
PSYQQ
PYCSY
RIG
RKO
RXVBD
S0X
SJFOW
SV3
TN5
UJ6
UKHRP
UQL
VH1
VQA
XJT
XOL
ZGI
ZXP
ZY4
~02
ID FETCH-LOGICAL-c341t-4d2e71f70bbcc86002c97838bf72cfae765d9bc86d5556388f5a311b768c80af2
IngestDate Sat Sep 28 08:46:37 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Keywords Cerebellum
Mesencephalon
Lizard
Telencephalon
Optic tectum
Rhombencephalon
Cognition
Ecomorph
Reptile
Mosaic evolution
Magnetic resonance imaging
Diencephalon
Tegmentum
Concerted evolution
Language English
License 2017 S. Karger AG, Basel.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c341t-4d2e71f70bbcc86002c97838bf72cfae765d9bc86d5556388f5a311b768c80af2
OpenAccessLink https://www.karger.com/Article/Pdf/478738
PMID 28869944
ParticipantIDs pubmed_primary_28869944
PublicationCentury 2000
PublicationDate 2017-01-01
PublicationDateYYYYMMDD 2017-01-01
PublicationDate_xml – month: 01
  year: 2017
  text: 2017-01-01
  day: 01
PublicationDecade 2010
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Brain, behavior and evolution
PublicationTitleAlternate Brain Behav Evol
PublicationYear 2017
SSID ssj0004241
Score 2.352305
Snippet The brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can...
SourceID pubmed
SourceType Index Database
StartPage 211
SubjectTerms Animals
Biological Evolution
Body Size
Brain - anatomy & histology
Brain - physiology
Ecology
Ecosystem
Lizards - anatomy & histology
Lizards - physiology
Magnetic Resonance Angiography - veterinary
Organ Size
Phylogeny
Species Specificity
Structure-Activity Relationship
Title Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards
URI https://www.ncbi.nlm.nih.gov/pubmed/28869944
Volume 90
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1bT9swFLbK0CRe0MY2YBfkB96mbLk4sf04tQWEoE90QntBtmNPlUqCQrVp_fU7voWCugl4iVxbiax8X06Pj893jNCh5KWo4a8lESolCWFKJKyqwJErJU9NVRDlziE7n1QnU3J6WV4OBr9X1SUL-UUt1-pKnoMq9AGuViX7BGT7h0IHtAFfuALCcH0UxvFIUJcrOLQCxM46kC53or0VMwXQwcr_8_hXmIaNbow68RNaZ7Ol1Vvd29TthK8oELX77kk63twzoG397oGXp8fu77NazJNj-HDc5vtIBCnQojf80_n8Op7JrDurYzm6k5edisbnCfkUy6CGCPGIjK7EI7S3ocRmfVBffSkaWX8maCBTcc9iZustecl96qOtHuQLwKwgenPtIM0Zqzj3BST_P_qgqHYc2kAblFnDOLFBniinBa8mFKGCWXzt52ALR4f7HixCnDNy8Qpth1UE_uYp8RoNdLODXo5dBfI_0PrRutYbNIwUwUAR3FMEA7DYUwQ71HFPEQw_PEVwoMhbND0aXwxPknBuRqLAJ1kkpM41zQxNpVSK2Y1XZQN8TBqaKyM0rcqaSxipS1sejjFTiiLLJKw8FUuFyd-hF03b6D2ESa40pdwUBSsJqWqecZUykipjVMplto92_Xu4uvHFUa7iG3r_z5EPaOuONx_RpoGvUX8C124hDxwQfwGbsksr
link.rule.ids 786
linkProvider National Library of Medicine
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Evidence+for+Concerted+and+Mosaic+Brain+Evolution+in+Dragon+Lizards&rft.jtitle=Brain%2C+behavior+and+evolution&rft.au=Hoops%2C+Daniel&rft.au=Vidal-Garc%C3%ADa%2C+Marta&rft.au=Ullmann%2C+Jeremy+F+P&rft.au=Janke%2C+Andrew+L&rft.date=2017-01-01&rft.eissn=1421-9743&rft.volume=90&rft.issue=3&rft.spage=211&rft_id=info:doi/10.1159%2F000478738&rft_id=info%3Apmid%2F28869944&rft_id=info%3Apmid%2F28869944&rft.externalDocID=28869944