How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation

One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS computational biology Jg. 13; H. 4; S. e1005358
Hauptverfasser: Kouvaris, Kostas, Clune, Jeff, Kounios, Loizos, Brede, Markus, Watson, Richard A.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Public Library of Science 01.04.2017
Public Library of Science (PLoS)
Schlagworte:
ISSN:1553-7358, 1553-734X, 1553-7358
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
Abstract One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting 'quick fixes' (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability.
AbstractList One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting ‘quick fixes’ (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability.
One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting 'quick fixes' (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability.One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting 'quick fixes' (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability.
One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting ‘quick fixes’ (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability. A striking feature of evolving organisms is their ability to acquire novel characteristics that help them adapt in new environments. The origin and the conditions of such ability remain elusive and is a long-standing question in evolutionary biology. Recent theory suggests that organisms can evolve designs that help them generate novel features that are more likely to be beneficial. Specifically, this is possible when the environments that organisms are exposed to share common regularities. However, the organisms develop robust designs that tend to produce what had been selected in the past and might be inflexible for future environments. The resolution comes from a recent theory introduced by Watson and Szathmáry that suggests a deep analogy between learning and evolution. Accordingly, here we utilise learning theory to explain the conditions that lead to more evolvable designs. We successfully demonstrate this by equating evolvability to the way humans and machines generalise to previously-unseen situations. Specifically, we show that the same conditions that enhance generalisation in learning systems have biological analogues and help us understand why environmental noise and the reproductive and maintenance costs of gene-regulatory connections can lead to more evolvable designs.
Audience Academic
Author Kounios, Loizos
Watson, Richard A.
Kouvaris, Kostas
Clune, Jeff
Brede, Markus
AuthorAffiliation University of Chicago, UNITED STATES
1 ECS, University of Southampton, Southampton, United Kingdom
2 University of Wyoming, Laramie, Wyoming, United States of America
AuthorAffiliation_xml – name: 1 ECS, University of Southampton, Southampton, United Kingdom
– name: 2 University of Wyoming, Laramie, Wyoming, United States of America
– name: University of Chicago, UNITED STATES
Author_xml – sequence: 1
  givenname: Kostas
  surname: Kouvaris
  fullname: Kouvaris, Kostas
– sequence: 2
  givenname: Jeff
  surname: Clune
  fullname: Clune, Jeff
– sequence: 3
  givenname: Loizos
  orcidid: 0000-0002-9133-9178
  surname: Kounios
  fullname: Kounios, Loizos
– sequence: 4
  givenname: Markus
  surname: Brede
  fullname: Brede, Markus
– sequence: 5
  givenname: Richard A.
  surname: Watson
  fullname: Watson, Richard A.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28384156$$D View this record in MEDLINE/PubMed
BookMark eNqVk81u1DAQxyNURD_gDRBE4lIOu9hxnI8ekKoK6EoVSFDOluNMUq-89tZOFvoAfW8mmyx0K4SEcsho5jd_z4xmjqMD6yxE0UtK5pTl9N3S9d5KM1-rSs8pIZzx4kl0RDlnsxztgwf2YXQcwpIQNMvsWXSYFKxIKc-OovtL9yOGjTN9p52NDUhvQ9y5uAULXhod4Cz-HrRt4-4G4rXXVum1gRC7ZqSnkPN3Q1pva_Chk7be8n-UEa9hA8atV2A7aWLnW2l1kEP0efS0kSbAi-l_El1__HB9cTm7-vJpcXF-NVMZY92shhzKlNUcOKmzrMhUQlJJSN1wVSmeNHVFaUV5WWKjWZkzgu5E8gyahBYVO4lej7Jr44KYBhgELTCBpVnGkViMRO3kUmC3K-nvhJNabB1Ys5C-08qAyGSiEs4ULXmSQoPVQMIB8gIgbShvUOv99FpfraBW2DYOdE90P2L1jWjdRnBWMEKHYk4nAe9uewidWOmgwBhpwfVD3QUv0zRhCaJvHqF_724-Uq3EBrRtHL6r8KthpRWuV6PRf56WLGdslH27l4BMBz-7VvYhiMW3r__Bft5nXz0cze-Z7PYSgbMRUN6F4KERSnfbVcGKtRGUiOEIdl2K4QjEdASYnD5K3un_M-0XrisPoQ
CitedBy_id crossref_primary_10_1162_artl_a_00354
crossref_primary_10_3390_app12094528
crossref_primary_10_3390_e26090765
crossref_primary_10_1073_pnas_1821066116
crossref_primary_10_1186_s13062_020_00277_0
crossref_primary_10_1007_s11406_020_00269_4
crossref_primary_10_1371_journal_pcbi_1006811
crossref_primary_10_1534_genetics_118_300995
crossref_primary_10_3390_biology6040042
crossref_primary_10_1038_s41598_023_47165_x
crossref_primary_10_1089_soro_2022_0142
crossref_primary_10_1111_ede_12374
crossref_primary_10_1371_journal_pcbi_1008425
crossref_primary_10_3389_fcell_2024_1453566
crossref_primary_10_1002_bies_70027
crossref_primary_10_1007_s13752_023_00447_z
crossref_primary_10_3389_fpsyg_2023_1330345
crossref_primary_10_1162_artl_a_00319
crossref_primary_10_1016_j_jtbi_2024_112032
crossref_primary_10_1016_j_tig_2025_01_008
crossref_primary_10_1093_nc_niab013
crossref_primary_10_1098_rsos_190202
crossref_primary_10_1038_s41467_021_21757_5
crossref_primary_10_1371_journal_pcbi_1006260
crossref_primary_10_3389_fevo_2022_823588
crossref_primary_10_1007_s12551_022_01018_5
crossref_primary_10_1038_s41467_025_57642_8
crossref_primary_10_3389_fnsys_2022_768201
crossref_primary_10_1038_s41539_025_00318_1
crossref_primary_10_7554_eLife_57468
crossref_primary_10_1111_ede_12309
crossref_primary_10_3390_biomimetics8010110
crossref_primary_10_1093_icb_icaa116
crossref_primary_10_1093_icb_icaa038
crossref_primary_10_12688_f1000research_11911_2
crossref_primary_10_3389_fpsyg_2019_02688
crossref_primary_10_7717_peerj_17102
crossref_primary_10_1002_bies_202100255
crossref_primary_10_1007_s00018_023_04790_z
crossref_primary_10_1038_s41598_022_05392_8
crossref_primary_10_1007_s42235_025_00756_y
crossref_primary_10_3390_e25010131
crossref_primary_10_1007_s13752_019_00325_7
crossref_primary_10_1093_biolinnean_blz064
crossref_primary_10_1038_s41598_021_91489_5
crossref_primary_10_1016_j_tig_2025_04_002
crossref_primary_10_1080_19420889_2023_2196145
Cites_doi 10.1002/jez.b.22597
10.1096/fj.00-0361com
10.1111/j.0014-3820.2002.tb01466.x
10.1038/nature03842
10.1073/pnas.97.9.4463
10.1101/gr.097378.109
10.1073/pnas.95.15.8420
10.1371/journal.pgen.1000877
10.1073/pnas.0701035104
10.1007/s10539-007-9089-3
10.1214/aos/1176344136
10.1073/pnas.0305212101
10.1073/pnas.0503610102
10.1007/s11692-011-9136-5
10.1162/106454600300103683
10.1098/rspb.2012.2863
10.1093/oso/9780195079517.001.0001
10.1016/j.tree.2006.05.001
10.1109/TAC.1974.1100705
10.1074/jbc.M104391200
10.1162/evco.1998.6.4.293
10.1038/nrg2267
10.1016/j.biosystems.2007.03.004
10.1086/414425
10.1186/1745-6150-8-24
10.1146/annurev-ecolsys-120213-091721
10.1073/pnas.1012918108
10.1111/evo.12337
10.1038/nrg2278
10.1007/s10618-008-0097-y
10.1007/978-1-4020-9636-5_8
10.1038/msb.2008.52
10.1109/IJCNN.2012.6252640
10.3905/jod.1997.407985
10.1371/journal.pone.0070444
10.1016/S0303-2647(02)00132-6
10.1046/j.1525-142x.2001.003002073.x
10.1016/0303-2647(79)90009-1
10.1073/pnas.0611630104
10.2307/2410639
10.1017/S0140525X06009010
10.1371/journal.pcbi.1000206
10.1038/npg.els.0004214
10.1073/pnas.0803596105
10.1007/978-3-642-03942-3
10.1016/j.tig.2010.06.002
10.1371/journal.pcbi.1000355
10.1016/j.jtbi.2006.10.027
10.1073/pnas.0409186102
10.2307/2410642
10.1038/nature08694
10.1145/2464576.2464597
10.1371/journal.pone.0038025
10.1038/nature01568
10.1371/journal.pcbi.1004829
ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kouvaris K, Clune J, Kounios L, Brede M, Watson RA (2017) How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comput Biol 13(4): e1005358. https://doi.org/10.1371/journal.pcbi.1005358
2017 Kouvaris et al 2017 Kouvaris et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kouvaris K, Clune J, Kounios L, Brede M, Watson RA (2017) How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comput Biol 13(4): e1005358. https://doi.org/10.1371/journal.pcbi.1005358
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kouvaris K, Clune J, Kounios L, Brede M, Watson RA (2017) How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comput Biol 13(4): e1005358. https://doi.org/10.1371/journal.pcbi.1005358
– notice: 2017 Kouvaris et al 2017 Kouvaris et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kouvaris K, Clune J, Kounios L, Brede M, Watson RA (2017) How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comput Biol 13(4): e1005358. https://doi.org/10.1371/journal.pcbi.1005358
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
ISN
ISR
3V.
7QO
7QP
7TK
7TM
7X7
7XB
88E
8AL
8FD
8FE
8FG
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
ARAPS
AZQEC
BBNVY
BENPR
BGLVJ
BHPHI
CCPQU
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
HCIFZ
JQ2
K7-
K9.
LK8
M0N
M0S
M1P
M7P
P5Z
P62
P64
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
Q9U
RC3
7X8
5PM
DOA
DOI 10.1371/journal.pcbi.1005358
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Canada
Gale In Context: Science
ProQuest Central (Corporate)
Biotechnology Research Abstracts
Calcium & Calcified Tissue Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Computing Database (Alumni Edition)
Technology Research Database
ProQuest SciTech Collection
ProQuest Technology Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
Advanced Technologies & Computer Science Collection
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Technology collection
Natural Science Collection
ProQuest One Community College
ProQuest Central
Engineering Research Database
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Computer Science Collection
Computer Science Database
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
Computing Database
Health & Medical Collection (Alumni Edition)
PML(ProQuest Medical Library)
Biological Science Database
Advanced Technologies & Aerospace Database
ProQuest Advanced Technologies & Aerospace Collection
Biotechnology and BioEngineering Abstracts
ProQuest Central Premium
ProQuest One Academic
ProQuest Publicly Available Content
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic (retired)
ProQuest One Academic UKI Edition
ProQuest Central China
ProQuest Central Basic
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
Computer Science Database
ProQuest Central Student
ProQuest Advanced Technologies & Aerospace Collection
ProQuest Central Essentials
ProQuest Computer Science Collection
Nucleic Acids Abstracts
SciTech Premium Collection
ProQuest Central China
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
Health Research Premium Collection
Natural Science Collection
Health & Medical Research Collection
Biological Science Collection
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Advanced Technologies & Aerospace Collection
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
ProQuest Technology Collection
Health Research Premium Collection (Alumni)
Biological Science Database
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
ProQuest Health & Medical Complete
ProQuest One Academic UKI Edition
Engineering Research Database
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
ProQuest One Academic (New)
Technology Collection
Technology Research Database
ProQuest One Academic Middle East (New)
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central
ProQuest Health & Medical Research Collection
Genetics Abstracts
Biotechnology Research Abstracts
Health and Medicine Complete (Alumni Edition)
ProQuest Central Korea
ProQuest Computing
ProQuest Central Basic
ProQuest Computing (Alumni Edition)
ProQuest SciTech Collection
Advanced Technologies & Aerospace Database
ProQuest Medical Library
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList Publicly Available Content Database
MEDLINE - Academic

MEDLINE



Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: PIMPY
  name: ProQuest Publicly Available Content
  url: http://search.proquest.com/publiccontent
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate How evolution learns to generalise
EISSN 1553-7358
ExternalDocumentID 1899334665
oai_doaj_org_article_6a2c253c19524ef686e25ee78ee4f15f
PMC5383015
A493733232
28384156
10_1371_journal_pcbi_1005358
Genre Research Support, U.S. Gov't, Non-P.H.S
Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FG
8FH
8FI
8FJ
AAFWJ
AAKPC
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACCTH
ACGFO
ACIHN
ACIWK
ACPRK
ACUHS
ADBBV
ADRAZ
AEAQA
AENEX
AEUYN
AFFHD
AFKRA
AFPKN
AFRAH
AHMBA
ALMA_UNASSIGNED_HOLDINGS
AOIJS
ARAPS
AZQEC
B0M
BAIFH
BAWUL
BBNVY
BBTPI
BCNDV
BENPR
BGLVJ
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DWQXO
E3Z
EAP
EAS
EBD
EBS
EJD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IGS
INH
INR
ISN
ISR
ITC
J9A
K6V
K7-
KQ8
LK8
M1P
M48
M7P
O5R
O5S
OK1
OVT
P2P
P62
PHGZM
PHGZT
PIMPY
PJZUB
PPXIY
PQGLB
PQQKQ
PROAC
PSQYO
PV9
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
XSB
~8M
ALIPV
C1A
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
NPM
RIG
WOQ
3V.
7QO
7QP
7TK
7TM
7XB
8AL
8FD
8FK
FR3
JQ2
K9.
M0N
P64
PKEHL
PQEST
PQUKI
PRINS
Q9U
RC3
7X8
5PM
AAPBV
ABPTK
M~E
N95
UMP
ID FETCH-LOGICAL-c633t-de7e943d5e50d6686c204a00df5cbc52fdb11b159935869730cbc2a56ef218b3
IEDL.DBID DOA
ISICitedReferencesCount 54
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000402542900002&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1553-7358
1553-734X
IngestDate Sun May 07 16:29:13 EDT 2023
Fri Oct 03 12:39:38 EDT 2025
Tue Nov 04 01:52:30 EST 2025
Sun Nov 09 11:41:19 EST 2025
Sat Nov 29 14:41:25 EST 2025
Tue Nov 04 17:56:18 EST 2025
Thu Nov 13 14:57:45 EST 2025
Thu Nov 13 15:00:36 EST 2025
Mon Jul 21 05:38:35 EDT 2025
Tue Nov 18 21:29:07 EST 2025
Sat Nov 29 06:01:26 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 4
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c633t-de7e943d5e50d6686c204a00df5cbc52fdb11b159935869730cbc2a56ef218b3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
Conceived and designed the experiments: RAW KK JC.Performed the experiments: KK.Analyzed the data: KK RAW MB LK.Wrote the paper: KK RAW JC MB LK.
The authors have declared that no competing interests exist.
ORCID 0000-0002-9133-9178
OpenAccessLink https://doaj.org/article/6a2c253c19524ef686e25ee78ee4f15f
PMID 28384156
PQID 1899334665
PQPubID 1436340
ParticipantIDs plos_journals_1899334665
doaj_primary_oai_doaj_org_article_6a2c253c19524ef686e25ee78ee4f15f
pubmedcentral_primary_oai_pubmedcentral_nih_gov_5383015
proquest_miscellaneous_1885944232
proquest_journals_1899334665
gale_infotracacademiconefile_A493733232
gale_incontextgauss_ISR_A493733232
gale_incontextgauss_ISN_A493733232
pubmed_primary_28384156
crossref_citationtrail_10_1371_journal_pcbi_1005358
crossref_primary_10_1371_journal_pcbi_1005358
PublicationCentury 2000
PublicationDate 2017-04-01
PublicationDateYYYYMMDD 2017-04-01
PublicationDate_xml – month: 04
  year: 2017
  text: 2017-04-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS computational biology
PublicationTitleAlternate PLoS Comput Biol
PublicationYear 2017
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References M Pavličev (ref26) 2015; 46
J Masel (ref62) 2010; 26
G Forman (ref69) 2008; 17
ref59
N Kashtan (ref64) 2009; 5
ref14
ref55
JL Fierst (ref40) 2015; 324
G Schwarz (ref58) 1978; 6
F Jacob (ref33) 1977
T Friedlander (ref44) 2013; 8
R Riedl (ref12) 1978
L Altenberg (ref13) 1995
LY Yampolsky (ref21) 2001; 3
TF Hansen (ref22) 2003; 69
C Adami (ref2) 2000; 97
C Braendle (ref18) 2010; 6
A Wagner (ref37) 1996
H Lipson (ref41) 2002; 56
GF Striedter (ref66) 2006; 29
ME Palmer (ref61) 2012; 7
N Kashtan (ref35) 2005; 102
X Gu (ref54) 2005; 102
J Vohradský (ref39) 2001; 15
LT MacNeil (ref50) 2011; 21
MA Bedau (ref1) 2000; 6
RD Leclerc (ref56) 2008; 4
GP Wagner (ref6) 1996
GP Wagner (ref29) 2007; 8
S Russell (ref68) 1995; 25
J Clune (ref27) 2013; 280
M Conrad (ref20) 1998
YS Abu-Mostafa (ref52) 2012
M Parter (ref34) 2008; 4
M Pavlicev (ref24) 2011; 38
M Pavlicev (ref23) 2010
S Galanti (ref70) 1997; 5
RE Lenski (ref3) 2003; 423
C Cherniak (ref67) 2004; 101
CD Schlichting (ref9) 2004
RA Watson (ref42) 2015
M Conrad (ref7) 1979; 11
J Vohradský (ref38) 2001; 276
MW Kirschner (ref8) 1998; 95
M Conrad (ref10) 1972; 4
CM Bishop (ref51) 2006; vol. 1
T Soule (ref60) 1998; 6
M Toussaint (ref17) 2007; 90
JA Draghi (ref31) 2010; 463
M Aldana (ref47) 2007; 245
SA Kauffman (ref53) 1993
MA Bedau (ref4) 2009
RA Watson (ref25) 2014; 68
E Rajon (ref63) 2011; 108
H Akaike (ref57) 1974; 19
ref28
RA Watson (ref43) 2015
J Gerhart (ref16) 2007; 104
N Kashtan (ref36) 2007; 104
A Livnat (ref45) 2013; 8
E Dekel (ref65) 2005; 436
I Brigandt (ref30) 2007; 22
J Matoušek (ref71) 1999
PM Brakefield (ref15) 2006; 21
MW Kirschner (ref32) 2006
A Livnat (ref46) 2008; 105
JM Smith (ref19) 1985
H Mengistu (ref48) 2016; 12
AP Moczek (ref5) 2011
M Pigliucci (ref11) 2008; 9
W Arthur (ref49) 2006
References_xml – volume: 324
  start-page: 1
  issue: 1
  year: 2015
  ident: ref40
  article-title: Modeling the evolution of complex genetic systems: The gene network family tree
  publication-title: Journal of Experimental Zoology Part B: Molecular and Developmental Evolution
  doi: 10.1002/jez.b.22597
– volume: 15
  start-page: 846
  issue: 3
  year: 2001
  ident: ref39
  article-title: Neural network model of gene expression
  publication-title: The FASEB Journal
  doi: 10.1096/fj.00-0361com
– volume: 56
  start-page: 1549
  issue: 8
  year: 2002
  ident: ref41
  article-title: On the origin of modular variation
  publication-title: Evolution
  doi: 10.1111/j.0014-3820.2002.tb01466.x
– volume: 436
  start-page: 588
  issue: 7050
  year: 2005
  ident: ref65
  article-title: Optimality and evolutionary tuning of the expression level of a protein
  publication-title: Nature
  doi: 10.1038/nature03842
– year: 1977
  ident: ref33
  article-title: Evolution and tinkering
  publication-title: Science
– volume: 97
  start-page: 4463
  issue: 9
  year: 2000
  ident: ref2
  article-title: Evolution of biological complexity
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.97.9.4463
– volume: 21
  start-page: 645
  issue: 5
  year: 2011
  ident: ref50
  article-title: Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression
  publication-title: Genome research
  doi: 10.1101/gr.097378.109
– volume: 95
  start-page: 8420
  issue: 15
  year: 1998
  ident: ref8
  article-title: Evolvability
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.95.15.8420
– volume: 6
  start-page: e1000877
  issue: 3
  year: 2010
  ident: ref18
  article-title: Bias and evolution of the mutationally accessible phenotypic space in a developmental system
  publication-title: PLoS genetics
  doi: 10.1371/journal.pgen.1000877
– volume: 104
  start-page: 8582
  issue: suppl 1
  year: 2007
  ident: ref16
  article-title: The theory of facilitated variation
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.0701035104
– volume: 22
  start-page: 709
  issue: 5
  year: 2007
  ident: ref30
  article-title: Typology now: homology and developmental constraints explain evolvability
  publication-title: Biology & Philosophy
  doi: 10.1007/s10539-007-9089-3
– volume: 6
  start-page: 461
  issue: 2
  year: 1978
  ident: ref58
  article-title: Estimating the dimension of a model
  publication-title: The annals of statistics
  doi: 10.1214/aos/1176344136
– volume: 101
  start-page: 1081
  issue: 4
  year: 2004
  ident: ref67
  article-title: Global optimization of cerebral cortex layout
  publication-title: Proceedings of the National Academy of Sciences of the United States of America
  doi: 10.1073/pnas.0305212101
– volume: 102
  start-page: 13773
  issue: 39
  year: 2005
  ident: ref35
  article-title: Spontaneous evolution of modularity and network motifs
  publication-title: Proceedings of the National Academy of Sciences of the United States of America
  doi: 10.1073/pnas.0503610102
– volume: 38
  start-page: 371
  issue: 4
  year: 2011
  ident: ref24
  article-title: Genotype-phenotype maps maximizing evolvability: Modularity revisited
  publication-title: Evolutionary Biology
  doi: 10.1007/s11692-011-9136-5
– volume: 6
  start-page: 363
  issue: 4
  year: 2000
  ident: ref1
  article-title: Open problems in artificial life
  publication-title: Artificial life
  doi: 10.1162/106454600300103683
– volume: 280
  start-page: 20122863
  issue: 1755
  year: 2013
  ident: ref27
  article-title: The evolutionary origins of modularity
  publication-title: Proceedings of the Royal Society b: Biological sciences
  doi: 10.1098/rspb.2012.2863
– year: 2011
  ident: ref5
  article-title: The role of developmental plasticity in evolutionary innovation
  publication-title: Proceedings of the Royal Society B: Biological Sciences
– year: 1993
  ident: ref53
  article-title: The origins of order: Self-organization and selection in evolution
  doi: 10.1093/oso/9780195079517.001.0001
– volume: 21
  start-page: 362
  issue: 7
  year: 2006
  ident: ref15
  article-title: Evo-devo and constraints on selection
  publication-title: Trends in Ecology & Evolution
  doi: 10.1016/j.tree.2006.05.001
– volume: 19
  start-page: 716
  issue: 6
  year: 1974
  ident: ref57
  article-title: A new look at the statistical model identification
  publication-title: IEEE transactions on automatic control
  doi: 10.1109/TAC.1974.1100705
– volume: 276
  start-page: 36168
  issue: 39
  year: 2001
  ident: ref38
  article-title: Neural model of the genetic network
  publication-title: Journal of Biological Chemistry
  doi: 10.1074/jbc.M104391200
– volume: vol. 1
  year: 2006
  ident: ref51
  article-title: Pattern recognition and machine learning
– volume: 6
  start-page: 293
  issue: 4
  year: 1998
  ident: ref60
  article-title: Effects of code growth and parsimony pressure on populations in genetic programming
  publication-title: Evolutionary Computation
  doi: 10.1162/evco.1998.6.4.293
– volume: 8
  start-page: 921
  issue: 12
  year: 2007
  ident: ref29
  article-title: The road to modularity
  publication-title: Nature Reviews Genetics
  doi: 10.1038/nrg2267
– volume: 90
  start-page: 769
  issue: 3
  year: 2007
  ident: ref17
  article-title: Complex adaptation and system structure
  publication-title: BioSystems
  doi: 10.1016/j.biosystems.2007.03.004
– start-page: 33
  year: 1998
  ident: ref20
  article-title: Evolutionary systems
– year: 2015
  ident: ref43
  article-title: How can evolution learn?
  publication-title: Trends in Ecology and Evolution
– start-page: 265
  year: 1985
  ident: ref19
  article-title: Developmental constraints and evolution: a perspective from the Mountain Lake conference on development and evolution
  publication-title: Quarterly Review of Biology
  doi: 10.1086/414425
– volume: 8
  start-page: 1
  issue: 1
  year: 2013
  ident: ref45
  article-title: Interaction-based evolution: how natural selection and nonrandom mutation worktogether
  publication-title: Biology direct
  doi: 10.1186/1745-6150-8-24
– volume: 46
  issue: 1
  year: 2015
  ident: ref26
  article-title: Constraints Evolve: Context-Dependency of Gene Effects Allows Evolution of Pleiotropy
  publication-title: Annual Review of Ecology, Evolution, and Systematics
  doi: 10.1146/annurev-ecolsys-120213-091721
– volume: 108
  start-page: 1082
  issue: 3
  year: 2011
  ident: ref63
  article-title: Evolution of molecular error rates and the consequences for evolvability
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.1012918108
– volume: 68
  start-page: 1124
  issue: 4
  year: 2014
  ident: ref25
  article-title: The Evolution of Phenotypic Correlations and “Developmental Memory”
  publication-title: Evolution
  doi: 10.1111/evo.12337
– volume: 25
  start-page: 27
  year: 1995
  ident: ref68
  article-title: A modern approach
  publication-title: Artificial Intelligence Prentice-Hall, Egnlewood Cliffs
– volume: 9
  start-page: 75
  issue: 1
  year: 2008
  ident: ref11
  article-title: Is evolvability evolvable?
  publication-title: Nature Reviews Genetics
  doi: 10.1038/nrg2278
– volume: 17
  start-page: 164
  issue: 2
  year: 2008
  ident: ref69
  article-title: Quantifying counts and costs via classification
  publication-title: Data Mining and Knowledge Discovery
  doi: 10.1007/s10618-008-0097-y
– year: 2010
  ident: ref23
  article-title: Evolution of adaptive phenotypic variation patterns by direct selection for evolvability
  publication-title: Proceedings of the Royal Society B: Biological Sciences
– year: 2009
  ident: ref4
  article-title: The evolution of complexity
  doi: 10.1007/978-1-4020-9636-5_8
– start-page: 1
  year: 2015
  ident: ref42
  article-title: Evolutionary connectionism: algorithmic principles underlying the evolution of biological organisation in evo-devo, evo-eco and evolutionary transitions
  publication-title: Evolutionary Biology
– volume: 4
  issue: 1
  year: 2008
  ident: ref56
  article-title: Survival of the sparsest: robust gene networks are parsimonious
  publication-title: Molecular systems biology
  doi: 10.1038/msb.2008.52
– ident: ref59
  doi: 10.1109/IJCNN.2012.6252640
– volume: 5
  start-page: 63
  issue: 1
  year: 1997
  ident: ref70
  article-title: Low-discrepancy sequences: Monte Carlo simulation of option prices
  publication-title: The Journal of Derivatives
  doi: 10.3905/jod.1997.407985
– start-page: 18
  year: 2004
  ident: ref9
  article-title: Plant Adaptation: Molecular genetics and ecology
– volume: 4
  start-page: 222
  year: 1972
  ident: ref10
  article-title: The importance of molecular hierarchy in information processing
  publication-title: Towards a theoretical biology
– year: 2006
  ident: ref32
  article-title: The plausibility of life: Resolving Darwin’s dilemma
– volume: 8
  start-page: e70444
  issue: 8
  year: 2013
  ident: ref44
  article-title: Mutation rules and the evolution of sparseness and modularity in biological systems
  publication-title: PloS one
  doi: 10.1371/journal.pone.0070444
– year: 2012
  ident: ref52
  article-title: Learning from data
– volume: 69
  start-page: 83
  issue: 2
  year: 2003
  ident: ref22
  article-title: Is modularity necessary for evolvability?: Remarks on the relationship between pleiotropy and evolvability
  publication-title: Biosystems
  doi: 10.1016/S0303-2647(02)00132-6
– year: 1978
  ident: ref12
  article-title: Order in living organisms: a systems analysis of evolution
– volume: 3
  start-page: 73
  issue: 2
  year: 2001
  ident: ref21
  article-title: Bias in the introduction of variation as an orienting factor in evolution
  publication-title: Evolution & development
  doi: 10.1046/j.1525-142x.2001.003002073.x
– volume: 11
  start-page: 167
  issue: 2
  year: 1979
  ident: ref7
  article-title: Bootstrapping on the adaptive landscape
  publication-title: BioSystems
  doi: 10.1016/0303-2647(79)90009-1
– volume: 104
  start-page: 13711
  issue: 34
  year: 2007
  ident: ref36
  article-title: Varying environments can speed up evolution
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.0611630104
– start-page: 967
  year: 1996
  ident: ref6
  article-title: Perspective: Complex adaptations and the evolution of evolvability
  publication-title: Evolution
  doi: 10.2307/2410639
– volume: 29
  start-page: 1
  issue: 01
  year: 2006
  ident: ref66
  article-title: Précis of principles of brain evolution
  publication-title: Behavioral and Brain Sciences
  doi: 10.1017/S0140525X06009010
– ident: ref55
– volume: 4
  start-page: e1000206
  issue: 11
  year: 2008
  ident: ref34
  article-title: Facilitated variation: how evolution learns from past environments to generalize to new environments
  publication-title: PLoS Computational Biology
  doi: 10.1371/journal.pcbi.1000206
– year: 2006
  ident: ref49
  article-title: Evolutionary developmental biology: developmental bias and constraint
  publication-title: eLS
  doi: 10.1038/npg.els.0004214
– volume: 105
  start-page: 19803
  issue: 50
  year: 2008
  ident: ref46
  article-title: A mixability theory for the role of sex in evolution
  publication-title: Proceedings of the National Academy of Sciences
  doi: 10.1073/pnas.0803596105
– year: 1999
  ident: ref71
  article-title: Geometric discrepancy: An illustrated guide
  doi: 10.1007/978-3-642-03942-3
– volume: 26
  start-page: 406
  issue: 9
  year: 2010
  ident: ref62
  article-title: Robustness and evolvability
  publication-title: Trends in Genetics
  doi: 10.1016/j.tig.2010.06.002
– volume: 5
  start-page: e1000355
  issue: 4
  year: 2009
  ident: ref64
  article-title: An analytically solvable model for rapid evolution of modular structure
  publication-title: PLoS computational biology
  doi: 10.1371/journal.pcbi.1000355
– volume: 245
  start-page: 433
  issue: 3
  year: 2007
  ident: ref47
  article-title: Robustness and evolvability in genetic regulatory networks
  publication-title: Journal of theoretical biology
  doi: 10.1016/j.jtbi.2006.10.027
– volume: 102
  start-page: 707
  issue: 3
  year: 2005
  ident: ref54
  article-title: Rapid evolution of expression and regulatory divergences after yeast gene duplication
  publication-title: Proceedings of the National Academy of Sciences of the United States of America
  doi: 10.1073/pnas.0409186102
– start-page: 1008
  year: 1996
  ident: ref37
  article-title: Does evolutionary plasticity evolve?
  publication-title: Evolution
  doi: 10.2307/2410642
– volume: 463
  start-page: 353
  issue: 7279
  year: 2010
  ident: ref31
  article-title: Mutational robustness can facilitate adaptation
  publication-title: Nature
  doi: 10.1038/nature08694
– ident: ref28
  doi: 10.1145/2464576.2464597
– volume: 7
  start-page: e38025
  issue: 6
  year: 2012
  ident: ref61
  article-title: Survivability is more fundamental than evolvability
  publication-title: PloS one
  doi: 10.1371/journal.pone.0038025
– volume: 423
  start-page: 139
  issue: 6936
  year: 2003
  ident: ref3
  article-title: The evolutionary origin of complex features
  publication-title: Nature
  doi: 10.1038/nature01568
– volume: 12
  start-page: e1004829
  issue: 6
  year: 2016
  ident: ref48
  article-title: The evolutionary origins of hierarchy
  publication-title: PLOS Comput Biol
  doi: 10.1371/journal.pcbi.1004829
– start-page: 205
  year: 1995
  ident: ref13
  article-title: Evolution and biocomputation
– ident: ref14
SSID ssj0035896
Score 2.4910638
Snippet One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such...
SourceID plos
doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1005358
SubjectTerms Adaptation
Amplification
Artificial intelligence
Automatic control
Background noise
Biological Evolution
Biological research
Biology
Biology and Life Sciences
Brain
Careers
Cerebral cortex
Classification
Cliffs
Colleges & universities
Computational Biology
Computational neuroscience
Computer applications
Cortex
Data acquisition
Data collection
Data processing
Detectors
Environment
Evolution
Evolution & development
Evolutionary adaptation
Evolutionary biology
Flexibility
Gene duplication
Gene expression
Gene regulation
Genetic algorithms
Genetics
Genomes
Humans
Laboratories
Learning
Learning algorithms
Machine Learning
Mathematical analysis
Mathematical models
Models, Biological
Modularity
Monte Carlo simulation
Natural selection
Neural networks
Noise
Noise prediction
Optimization
Organisms
Origins
Pattern recognition
Phenotype
Phenotypic variations
Physical Sciences
Population genetics
Populations
Pressure
Probability theory
Ribonuclease
Securities prices
Selection, Genetic
Simulation
Social Sciences
Statistical analysis
Stochasticity
Technology
Theory
Variability
SummonAdditionalLinks – databaseName: Biological Science Database
  dbid: M7P
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lb9QwELZgAYlLedNAQQYhcQpN_ErCBRVEVS6rCnrYW5Q4drtSlYTNbqv-AP43M46TJajAgWs8tuzxePzFHs9HyBtMGaK4TcMCNsdQiATWHM9sCNiZxZUoC64KRzaRzOfpYpEd-wO3zodVDj7ROeqq0XhGvh_DjwHnQin5of0eImsU3q56Co2b5BZmSWAudO948MRcpo6fC6lxwoSLhX86x5N438_Uu1aXS4wUgC6nk63JZfAf_fSsPW-660Do77GUv2xOh_f-d1j3yY6HpfSgt6MH5IapH5I7PVHl1SPy46i5pObCmyl1VBMdXTf0tM9avezMe-qiDygAStoOJ_gdbSz1xBSuqFldYbXN-KTGyW9bBvFqG8YEPepZp_qQo8fk5PDzyaej0BM4hFpxvg4rk5hM8EoaGVVKpUqzSBRRVFmpSy2Zrco4LgFQ4WWsysDZwGdWSGUsII-SPyGzuqnNLqFcVmUEtSLLlTCxTpkueVzqMkljblQWED5MXa59cnPk2DjP3Y1dAj85vSJznPDcT3hAwrFW2yf3-If8R7SKURZTc7sPoIvcr_RcFUwzyXWcSSaMhVEbJo1JUmOEjaUNyGu0qRyTb9QY3XNabLou__Jtnh8IAIucA8j9o9DXidBbL2QbGKwu_IsKUBkm9ZpI7qIBD4Pq8q3ZBWRvMMzri1-NxeB48DapqE2zQZlUZkK41p_2a2BUDGDWFE8GApJMVsdEc9OSennmkpvDBgx7jnz29249J3cZ4isXQrVHZuvVxrwgt_XFetmtXjov8BMyqWjP
  priority: 102
  providerName: ProQuest
– databaseName: Public Library of Science (PLoS) Journals Open Access
  dbid: FPL
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1Lb9QwELZgAakX3tBAQQYhcQrEzyTcCmJVJLSqoIferNixy0pVstrstuoP4H8zdrxZUnWFuHrGlj0Zez5nxjMIvfMpQyRzRVqBcUw5z2HPsdKlgJ0pqbmumKxCsYl8NitOT8vj7UXxmgef5eRjlOmHhdFz79OHwYvb6A5lUvpSDdPj75uTFwiljM_jdvUcmZ-QpX84iyeL87a7CWhej5f8ywBNH_zv1B-i-xFq4sNeNx6hW7Z5jO71xSevnqDfR-0lthdR9XAoH9HhVYvP-kzU885-wiGiAANIxIvNX_kOtw7HYhOB1C6vfLf18Ewm8G9HBvZ6G5oEM-orSfVhRE_RyfTryZejNBZlSI1kbJXWNrclZ7WwIqulLKShGa-yrHbCaCOoqzUhGkCSd7DKEg4QaKaVkNYBmtDsGZo0bWP3EWai1hn0yhyT3BJTUKMZ0UbnBWFWlglim0-lTExY7utmnKvghcvh4tILUnn5qijfBKVDr0WfsOMf_J-9Fgy8Pt12aABZqLh7layooYIZUgrKrYNVWyqszQtruSPCJeit1yHlE2o0PmLnrFp3nfr2c6YOOQBAxgC47mT6MWJ6H5lcC4s1VXwlASLzibpGnPteYTeL6hSBqzNjXEqRoIONEt9MfjOQ4TDxHqKqse3a8xSi5DyM_rzX-UEwgEMLf9tPUD7aDSPJjSnN_FdIWA5GFeyIeLF7xi_RHvV4KYREHaDJarm2r9Bdc7Gad8vXYZf_AaIdVNQ
  priority: 102
  providerName: Public Library of Science
Title How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation
URI https://www.ncbi.nlm.nih.gov/pubmed/28384156
https://www.proquest.com/docview/1899334665
https://www.proquest.com/docview/1885944232
https://pubmed.ncbi.nlm.nih.gov/PMC5383015
https://doaj.org/article/6a2c253c19524ef686e25ee78ee4f15f
http://dx.doi.org/10.1371/journal.pcbi.1005358
Volume 13
WOSCitedRecordID wos000402542900002&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVAON
  databaseName: DOAJ Directory of Open Access Journals
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: DOA
  dateStart: 20050101
  isFulltext: true
  titleUrlDefault: https://www.doaj.org/
  providerName: Directory of Open Access Journals
– providerCode: PRVPQU
  databaseName: Advanced Technologies & Aerospace Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: P5Z
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/hightechjournals
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Biological Science Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: M7P
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/biologicalscijournals
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Computer Science Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: K7-
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/compscijour
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Health & Medical Collection
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: 7X7
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/healthcomplete
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest Central
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: BENPR
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://www.proquest.com/central
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest Publicly Available Content
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: PIMPY
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/publiccontent
  providerName: ProQuest
– providerCode: PRVATS
  databaseName: Public Library of Science (PLoS) Journals Open Access
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: FPL
  dateStart: 20050101
  isFulltext: true
  titleUrlDefault: http://www.plos.org/publications/
  providerName: Public Library of Science
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELZgAYkL4tkulJVBSJxCk_gZbi1q1QpYRaWHhUuUOHZZqUpWm92i_gD-N-PHpg0q6oWLD_Y4iseT8ed4_A1C7yxlCCdGRiUsjhGlAr45kpkIsHOa1LQqCS9dsgkxncrZLMuvpfqyMWGeHtgrbpeXqUoZUUnGUqoNl1ynTGshtaYmYcZ631hkm82U98GESZeZyybFiQShs3BpjohkN8zRh4Wq5jZGAF5WDhYlx93fe-jR4rztboKff0dRXluWDh-jRwFP4j0_jifojm6eogc-w-TlM_T7qP2F9UWwL-xyRHR41eIzTzc97_RH7MIGMCBBvNj8eu9wa3DIKOGa2uWl7bbu78I4-asng3h9FX8Eb-TTRflYoefo9PDg9NNRFDIvRIoTsopqLXRGSc00i2sOOldpTMs4rg1TlWKpqaskqQAJ2VNUnoGXgOq0ZFwbgAwVeYFGTdvobYQJq6sYesWGcKoTJVNVkaRSlZAJ0TwbI7LRfKECK7lNjnFeuKM2AbsTr8jCzlcR5muMor7XwrNy3CK_bye1l7Wc2q4CdFEESytus7QxemtNorCsGY0Nyzkr111XHH-bFnsUUB4hgE7_KXQyEHofhEwLg1VluAoBKrNsXAPJbWt_m0F1RQL7Y0Io52yMdjY2eXPzm74ZPIY9Biob3a6tjGQZpe7pW96Ee8UA2JR2Sz9GYmDcA80NW5r5T8dKDisnLBbs5f9Q9Sv0MLXwyUVI7aDRarnWr9F9dbGad8sJuitmwpVygu7tH0zzk4n7_KE8zL9A-VlEExvFm0OZsx8glR9_zb__ARlGY7Y
linkProvider Directory of Open Access Journals
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1Lb9QwELbKAoILb9qFAgaBegpN_EqChFB5VLtqWVWwh71ZiWO3K1XJstlttT-An8N_ZOw8lqACpx64xmMrnszLmfF8CL20LUMENZGXgHP0GAtB52hsPIidSZCxNKEicWAT4WgUTSbx0Qb60dyFsWWVjU10hjorlP1HvhvAwYBSJgR_N_vmWdQom11tIDQqsTjQq3M4spVvhx_h-74iZP_T-MPAq1EFPCUoXXiZDnXMaMY19zMhIqGIzxLfzwxXqeLEZGkQpODlbYZQxKAB8JgkXGgD7jClsOwVdBWiCOK7SsGjxvADuYMDs0g8XkjZpL6pR8NgtxaM1zOVTm1hAnAo6nhCBxjQuoXe7LQoL4p5fy_d_MUX7t_-z7h4B92qg268V2nJXbSh83voegXDubqPvg-Kc6zPaiXEDkijxIsCH1c9uaelfoNdbQWGcBnPmvxEiQuDa9gNN1TMV3basr0w5OjXKwN5ti7SgjeqMLWqgqoHaHwZLHiIenmR6y2EKc9SH2b5hgqmAxURldIgVWkYBVSLuI9oIylS1a3bLYLIqXT5yBCOcBUjpZUvWctXH3ntrFnVuuQf9O-tELa0tvG4ewC8kLUdkyIhinCqgpgTpg3sWhOudRhpzUzATR-9sCIsbWuR3NYuHSfLspTDryO5xyAUphRC-D8SfekQ7dREpoDNqqS-LwIssy3LOpRbVl-aTZVyLeV9tN3owcXDz9thMKs2V5bkulhamojHjLnVNyuVaxkDEXlk_3v0UdhRxg7nuiP59MS1bofwAjwqf_T313qGbgzGnw_l4XB08BjdJDaSdMVi26i3mC_1E3RNnS2m5fypM0AYyUtW1Z9S98S9
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1bb9MwFLZGuYgX7rDCAINAPIUmviVBQmgwqlVD1QR76JuVOPaoNCWlaTf1B_Cj-HccO05K0YCnPfAaH1vxybk55_h8CL2wLUMENUmQgXMMGItB52hqAoidSVSwPKMic2AT8XicTCbp4Rb60d6FsWWVrU10hrqolP1HPojgYEApE4IPjC-LONwbvpt9CyyClM20tnAajYgc6NUZHN_qt6M9-NYvCRl-PPqwH3iEgUAJShdBoWOdMlpwzcNCiEQoErIsDAvDVa44MUUeRTl4fJstFCloAzwmGRfagGvMKSx7CV2OmQiJqxo8bJ0AkDtoMIvKE8SUTfytPRpHAy8kr2cqn9oiBeBWsuEVHXhA5yJ6s5OqPi_-_b2M8xe_OLz5H3P0Frrhg3G822jPbbSlyzvoagPPubqLvu9XZ1ifeuXEDmCjxosKHze9uqe1foNdzQWGMBrP2rxFjSuDPRyHG6rmKztt2V0kcvTrlYG8WBdvwRs1WFtNodU9dHQRLLiPemVV6m2EKS_yEGaFhgqmI5UQldMoV3mcRFSLtI9oKzVS-ZbuFlnkRLo8ZQxHu4aR0sqa9LLWR0E3a9a0NPkH_XsrkB2tbUjuHgAvpLdvUmREEU5VlHLCtIFda8K1jhOtmYm46aPnVpylbTlSWlE7zpZ1LUdfxnKXQYhMKYT2fyT6vEH0yhOZCjarMn-PBFhmW5ltUG5b3Wk3Vcu1xPfRTqsT5w8_64bB3NocWlbqamlpEp4y5lZ_0KhfxxiI1BP7P6SP4g3F3ODc5kg5_epaukPYAZ6WP_z7az1F10BD5afR-OARuk5sgOlqyHZQbzFf6sfoijpdTOv5E2eLMJIXrKk_AaYzzYM
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=How+evolution+learns+to+generalise%3A+Using+the+principles+of+learning+theory+to+understand+the+evolution+of+developmental+organisation&rft.jtitle=PLoS+computational+biology&rft.au=Kouvaris%2C+Kostas&rft.au=Clune%2C+Jeff&rft.au=Kounios%2C+Loizos&rft.au=Brede%2C+Markus&rft.date=2017-04-01&rft.issn=1553-7358&rft.eissn=1553-7358&rft.volume=13&rft.issue=4&rft.spage=e1005358&rft_id=info:doi/10.1371%2Fjournal.pcbi.1005358&rft.externalDBID=n%2Fa&rft.externalDocID=10_1371_journal_pcbi_1005358
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7358&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7358&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7358&client=summon