The transcription factor Krüppel homolog 1is linked to hormone mediated social organization in bees

Abstract Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and faculta...

Full description

Saved in:
Bibliographic Details
Published inBMC evolutionary biology Vol. 10; no. 1; p. 1
Main Authors Shpigler, Hagai, Patch, Harland M, Cohen, Mira, Fan, Yongliang, Grozinger, Christina M, Bloch, Guy
Format Journal Article
LanguageEnglish
Published London BioMed Central 30.04.2010
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Abstract Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 ( Kr-h1 ), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera. Results In contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders. Conclusions Our results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.
AbstractList Abstract Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 ( Kr-h1 ), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera. Results In contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders. Conclusions Our results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.
Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 (Kr-h1), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera. Results In contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders. Conclusions Our results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.
ArticleNumber 120
Author Bloch, Guy
Shpigler, Hagai
Fan, Yongliang
Cohen, Mira
Grozinger, Christina M
Patch, Harland M
Author_xml – sequence: 1
  givenname: Hagai
  surname: Shpigler
  fullname: Shpigler, Hagai
– sequence: 2
  givenname: Harland M
  surname: Patch
  fullname: Patch, Harland M
– sequence: 3
  givenname: Mira
  surname: Cohen
  fullname: Cohen, Mira
– sequence: 4
  givenname: Yongliang
  surname: Fan
  fullname: Fan, Yongliang
– sequence: 5
  givenname: Christina M
  surname: Grozinger
  fullname: Grozinger, Christina M
– sequence: 6
  givenname: Guy
  surname: Bloch
  fullname: Bloch, Guy
BookMark eNpNkDFPwzAUhC1UJNrCzmiJOeDnJMQeUQUUUYmlzNGL7bQuiR3sdIDfxsYfI2kRYnqnT6d7p5uRifPOEHIJ7BpA3N5AVkDCIRMJsAQ4OyHTPzT5p8_ILMYdY1AIDlOi11tD-4AuqmC73npHa1S9D_Q5fH91nWno1re-8RsKNtLGujejae8HGtqhAW2NttgPLHplsaE-bNDZTzxEWUcrY-I5Oa2xiebi987J68P9erFMVi-PT4u7VaI4z1hSaciqKh-boTRacYlY8FQoYCjrGkFJqZjK0krnaLCAVBdMixREWhda6HROro65XfDvexP7cuf3wQ0vSy7zHETBuRxc7OhSwccYTF12wbYYPkpg5bhlOY5VjmMdCGfpD_eOak0
CitedBy_id crossref_primary_10_1038_srep00163
crossref_primary_10_1111_mec_13410
crossref_primary_10_1016_j_yhbeh_2020_104844
crossref_primary_10_1016_j_cois_2023_101115
crossref_primary_10_1111_mec_13198
crossref_primary_10_1007_s00265_016_2071_9
crossref_primary_10_1186_1471_2148_11_95
crossref_primary_10_1038_s41598_022_06715_5
crossref_primary_10_1016_j_jinsphys_2023_104557
crossref_primary_10_1111_j_1601_183X_2012_00782_x
crossref_primary_10_1016_j_cell_2021_10_006
crossref_primary_10_1016_j_yhbeh_2016_08_004
crossref_primary_10_1098_rstb_2010_0346
crossref_primary_10_1038_s42003_023_05273_4
crossref_primary_10_1242_jeb_217547
crossref_primary_10_1016_j_ydbio_2013_09_031
crossref_primary_10_1098_rstb_2019_0737
crossref_primary_10_3390_biology10111188
crossref_primary_10_1093_gbe_evad095
crossref_primary_10_1242_jeb_247516
crossref_primary_10_1016_j_cois_2015_09_006
crossref_primary_10_1126_science_aar5723
crossref_primary_10_1242_jeb_247396
crossref_primary_10_1098_rsos_160576
crossref_primary_10_1111_j_1365_2583_2012_01153_x
crossref_primary_10_3389_fphys_2022_905441
crossref_primary_10_1016_j_ijbiomac_2022_12_229
crossref_primary_10_1016_j_jinsphys_2017_08_001
crossref_primary_10_1098_rspb_2013_2419
crossref_primary_10_3389_fphys_2018_01677
crossref_primary_10_3389_fgene_2020_01027
crossref_primary_10_1016_j_yhbeh_2023_105330
crossref_primary_10_1371_journal_pone_0100650
crossref_primary_10_1007_s10886_017_0858_4
crossref_primary_10_1016_j_yhbeh_2019_104602
crossref_primary_10_1038_s41598_022_25675_4
crossref_primary_10_1186_1471_2148_14_45
crossref_primary_10_1242_jeb_107250
crossref_primary_10_1038_srep01570
crossref_primary_10_3389_fphys_2016_00574
Cites_doi 10.1186/1471-2164-9-232
10.1002/dneu.20537
10.1242/jeb.205.17.2567
10.1111/j.1096-0031.2001.tb00115.x
10.1002/neu.480260111
10.1006/hbeh.1999.1552
10.1007/BF00192722
10.1016/j.ydbio.2008.10.016
10.1007/978-1-59745-251-9_6
10.1016/S0022-1910(98)00040-7
10.1101/gr.5204306
10.1086/519965
10.1016/S0070-2153(06)74006-6
10.1111/j.1365-3032.1996.tb00863.x
10.1146/annurev.ento.52.110405.091434
10.1023/A:1020805103379
10.1016/S0070-2153(08)60364-6
10.1016/B978-012532104-4/50042-1
10.1126/science.1159277
10.1007/BF00296638
10.1073/pnas.2335884100
10.1016/j.mod.2007.10.002
10.1007/s00040-004-0741-5
10.1016/j.jinsphys.2005.03.009
10.1186/1741-7007-7-34
10.1163/156853988X00340
10.1007/s00114-008-0353-4
10.1093/aesa/83.3.626
10.1016/j.tree.2008.03.006
10.1007/s00114-006-0197-8
10.1016/j.mod.2008.03.004
10.1111/j.1365-294X.2007.03545.x
10.1098/rspb.1999.0947
10.1002/(SICI)1520-6327(1997)35:4<559::AID-ARCH13>3.0.CO;2-9
10.1016/S0022-1910(99)00101-8
10.1002/neu.10256
10.1007/PL00000885
10.1038/nrg1575
10.1007/s003590050426
10.1242/jeb.02125
10.1093/oxfordjournals.molbev.a003851
10.1006/anbe.1993.1092
10.1111/j.1570-7458.1989.tb01231.x
10.1007/s002650050546
10.1080/10635150390235520
10.1093/molbev/msm092
10.1016/j.jinsphys.2006.11.009
10.1007/978-3-0348-8878-3_13
10.1016/B978-008088783-8.00030-9
10.1127/entom.gen/29/2007/305
10.1111/j.1365-3032.1989.tb00954.x
10.1016/S0960-9822(01)00124-5
10.1016/j.bbr.2007.02.014
10.1163/002829687X00080
10.1111/j.1365-2311.1949.tb01420.x
10.1177/074873001129002123
10.1016/0022-1910(77)90126-3
10.1007/BF02224031
10.1007/s003590050423
10.1007/s00359-006-0202-x
10.1111/j.1365-2583.2008.00819.x
10.1007/s00265-006-0184-2
10.1016/j.tig.2007.05.001
ContentType Journal Article
Copyright 2010. This work is licensed under https://creativecommons.org/licenses/by/2.0 (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2010. This work is licensed under https://creativecommons.org/licenses/by/2.0 (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
DBID AAYXX
CITATION
3V.
7QP
7QR
7SN
7SS
7TK
7X7
7XB
88E
8FD
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
ATCPS
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
HCIFZ
K9.
LK8
M0S
M1P
M7P
P64
PATMY
PIMPY
PQEST
PQQKQ
PQUKI
PRINS
PYCSY
RC3
DOI 10.1186/1471-2148-10-120
DatabaseName CrossRef
ProQuest Central (Corporate)
Calcium & Calcified Tissue Abstracts
Chemoreception Abstracts
Ecology Abstracts
Entomology Abstracts (Full archive)
Neurosciences Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Technology Research Database
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central
Agricultural & Environmental Science Collection
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One Community College
ProQuest Central Korea
Engineering Research Database
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
Health & Medical Collection (Alumni Edition)
Medical Database
Biological Science Database
Biotechnology and BioEngineering Abstracts
Environmental Science Database
Publicly Available Content Database
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
Environmental Science Collection
Genetics Abstracts
DatabaseTitle CrossRef
Publicly Available Content Database
ProQuest Central Student
Technology Research Database
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Central China
Environmental Sciences and Pollution Management
ProQuest Central
Genetics Abstracts
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Agricultural & Environmental Science Collection
Biological Science Collection
Chemoreception Abstracts
ProQuest Medical Library (Alumni)
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
Ecology Abstracts
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
Environmental Science Collection
Entomology Abstracts
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
Environmental Science Database
Engineering Research Database
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
ProQuest Central (Alumni)
DatabaseTitleList CrossRef
Publicly Available Content Database
Database_xml – sequence: 1
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
Nursing
EISSN 1471-2148
ExternalDocumentID 10_1186_1471_2148_10_120
GroupedDBID ---
-A0
0R~
23N
2VQ
2WC
2XV
3V.
4.4
53G
5VS
6J9
7X7
7XC
88E
8CJ
8FE
8FH
8FI
8FJ
AAHBH
AAYXX
ABDBF
ABUWG
ACGFO
ACGFS
ACIHN
ACIWK
ACPRK
ADBBV
ADINQ
ADRAZ
AEAQA
AENEX
AFKRA
AFRAH
AHBYD
AHMBA
AHSBF
AHYZX
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AMKLP
AOIJS
ATCPS
BAWUL
BBNVY
BCNDV
BENPR
BFQNJ
BHPHI
BMC
BPHCQ
BVXVI
C1A
C24
C6C
CCPQU
CITATION
CS3
D1J
DIK
DU5
E3Z
EAD
EAP
EAS
EBD
EBS
EJD
EMB
EMK
EMOBN
ESX
F5P
FYUFA
GROUPED_DOAJ
GX1
H13
HCIFZ
HMCUK
HYE
IAO
IGS
IHR
INH
INR
IPNFZ
ISR
ITC
KQ8
LK8
M1P
M48
M7P
M~E
O5R
O5S
OK1
P2P
PATMY
PGMZT
PIMPY
PQQKQ
PROAC
PSQYO
PYCSY
RBZ
RIG
RNS
ROL
RPM
RSV
SBL
SOJ
SV3
TR2
TUS
U2A
UKHRP
WOQ
WOW
XSB
7QP
7QR
7SN
7SS
7TK
7XB
8FD
8FK
AZQEC
C1K
DWQXO
FR3
GNUQQ
K9.
P64
PQEST
PQUKI
PRINS
RC3
ID FETCH-LOGICAL-c2240-bd14bb51782a9edc29aa7238c10a9ffa1c99c0c43bd5aea713d70d83183f7d8d3
IEDL.DBID M48
ISSN 1471-2148
IngestDate Thu Oct 10 17:05:53 EDT 2024
Thu Sep 12 18:42:42 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c2240-bd14bb51782a9edc29aa7238c10a9ffa1c99c0c43bd5aea713d70d83183f7d8d3
OpenAccessLink https://www.proquest.com/docview/2955187229?pq-origsite=%requestingapplication%
PQID 2955187229
PQPubID 44659
ParticipantIDs proquest_journals_2955187229
crossref_primary_10_1186_1471_2148_10_120
PublicationCentury 2000
PublicationDate 2010-04-30
PublicationDateYYYYMMDD 2010-04-30
PublicationDate_xml – month: 04
  year: 2010
  text: 2010-04-30
  day: 30
PublicationDecade 2010
PublicationPlace London
PublicationPlace_xml – name: London
PublicationTitle BMC evolutionary biology
PublicationYear 2010
Publisher BioMed Central
Publisher_xml – name: BioMed Central
References HB Boudreaux (1336_CR70) 1979
SB Carroll (1336_CR50) 2005
BC Trainor (1336_CR9) 2007; 179
C Alaux (1336_CR14) 2004; 51
AB Barron (1336_CR63) 2007; 53
SE Fahrbach (1336_CR43) 2003; 57
G Bloch (1336_CR60) 1999; 266
GP Wagner (1336_CR33) 2008; 23
GE Robinson (1336_CR1) 2005; 6
G Bloch (1336_CR24) 1996; 21
SA Cameron (1336_CR27) 1990; 83
G Bloch (1336_CR56) 2001; 16
JP Sullivan (1336_CR22) 2000; 37
R Kraut (1336_CR49) 2001; 11
C Minakuchi (1336_CR46) 2008; 125
WC Wheeler (1336_CR69) 2001; 17
T Pankiw (1336_CR13) 1998; 44
CM Grozinger (1336_CR31) 2007; 193
L Shi (1336_CR45) 2007; 67
AL Toth (1336_CR51) 2007; 23
GS Withers (1336_CR44) 1995; 26
K Tamura (1336_CR68) 2007; 24
A Van Doorn (1336_CR26) 1989; 14
CM Grozinger (1336_CR30) 2007; 94
EO Wilson (1336_CR2) 1971
CD Michener (1336_CR3) 1974
1336_CR20
J Savard (1336_CR36) 2006; 16
RA Cumber (1336_CR39) 1949; 100
S Whelan (1336_CR72) 2001; 18
B Fussnecker (1336_CR42) 2008; 17
G Bloch (1336_CR23) 2000; 46
CM Grozinger (1336_CR32) 2003; 100
S Yerushalmi (1336_CR55) 2006; 209
W Hennig (1336_CR71) 1981
C Lopez-Vaamonde (1336_CR15) 2007
BM Wiegmann (1336_CR37) 2009; 7
EA Kravitz (1336_CR7) 2000; 186
G Bloch (1336_CR19) 2002
SD Kocher (1336_CR41) 2008; 9
J Cnaani (1336_CR57) 2007; 29
Y Le Conte (1336_CR12) 2008; 53
G Bloch (1336_CR29) 2009
L Keller (1336_CR5) 1993; 45
DH Edwards (1336_CR8) 2006; 74
C Minakuchi (1336_CR47) 2008; 325
TA Hall (1336_CR64) 1999; 41
R Gadagkar (1336_CR4) 1997
C Alaux (1336_CR16) 2006; 60
S Iuchi (1336_CR35) 2001; 58
R Parthasarathy (1336_CR48) 2008; 125
G Bloch (1336_CR38) 1999; 45
A Van Doorn (1336_CR62) 1986; 33
GE Robinson (1336_CR52) 1997; 35
MJ West-Eberhard (1336_CR53) 1996
A Van Doorn (1336_CR28) 1987; 37
MJ Duchateau (1336_CR34) 1989; 51
G Bloch (1336_CR17) 1999; 25
D Gotzek (1336_CR11) 2007; 82
S Geva (1336_CR59) 2005; 51
Z-Y Huang (1336_CR21) 1994; 174
S Guindon (1336_CR65) 2003; 52
A Sramkova (1336_CR18) 2008; 95
CM Grozinger (1336_CR40) 2007; 16
PF Roseler (1336_CR25) 1977; 23
MJ Duchateau (1336_CR61) 1988; 107
G Bloch (1336_CR58) 2000; 186
S Guindon (1336_CR66) 2009; 537
K Hartfelder (1336_CR54) 1998; 40
DT Jones (1336_CR67) 1992; 8
GE Robinson (1336_CR6) 2008; 322
SA White (1336_CR10) 2002; 205
References_xml – volume: 9
  start-page: 232
  year: 2008
  ident: 1336_CR41
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-9-232
  contributor:
    fullname: SD Kocher
– volume: 67
  start-page: 1614
  year: 2007
  ident: 1336_CR45
  publication-title: Dev Neurobiol
  doi: 10.1002/dneu.20537
  contributor:
    fullname: L Shi
– volume: 205
  start-page: 2567
  issue: Pt 17
  year: 2002
  ident: 1336_CR10
  publication-title: J Exp Biol
  doi: 10.1242/jeb.205.17.2567
  contributor:
    fullname: SA White
– volume: 17
  start-page: 113
  year: 2001
  ident: 1336_CR69
  publication-title: Cladistics
  doi: 10.1111/j.1096-0031.2001.tb00115.x
  contributor:
    fullname: WC Wheeler
– volume: 26
  start-page: 130
  year: 1995
  ident: 1336_CR44
  publication-title: J Neurobiol
  doi: 10.1002/neu.480260111
  contributor:
    fullname: GS Withers
– volume: 37
  start-page: 1
  issue: 1
  year: 2000
  ident: 1336_CR22
  publication-title: Horm Behav
  doi: 10.1006/hbeh.1999.1552
  contributor:
    fullname: JP Sullivan
– volume: 174
  start-page: 731
  year: 1994
  ident: 1336_CR21
  publication-title: J Comp Physiol [A]
  doi: 10.1007/BF00192722
  contributor:
    fullname: Z-Y Huang
– volume: 325
  start-page: 341
  year: 2008
  ident: 1336_CR47
  publication-title: Dev Biol
  doi: 10.1016/j.ydbio.2008.10.016
  contributor:
    fullname: C Minakuchi
– volume: 537
  start-page: 113
  year: 2009
  ident: 1336_CR66
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-59745-251-9_6
  contributor:
    fullname: S Guindon
– volume: 44
  start-page: 685
  issue: 7-8
  year: 1998
  ident: 1336_CR13
  publication-title: J Insect Physiol
  doi: 10.1016/S0022-1910(98)00040-7
  contributor:
    fullname: T Pankiw
– volume: 16
  start-page: 1334
  year: 2006
  ident: 1336_CR36
  publication-title: Genome Res
  doi: 10.1101/gr.5204306
  contributor:
    fullname: J Savard
– volume: 82
  start-page: 201
  issue: 3
  year: 2007
  ident: 1336_CR11
  publication-title: Q Rev Biol
  doi: 10.1086/519965
  contributor:
    fullname: D Gotzek
– volume: 74
  start-page: 177
  year: 2006
  ident: 1336_CR8
  publication-title: Curr Top Dev Biol
  doi: 10.1016/S0070-2153(06)74006-6
  contributor:
    fullname: DH Edwards
– volume: 21
  start-page: 257
  year: 1996
  ident: 1336_CR24
  publication-title: Physiological Entomology
  doi: 10.1111/j.1365-3032.1996.tb00863.x
  contributor:
    fullname: G Bloch
– volume: 53
  start-page: 523
  year: 2008
  ident: 1336_CR12
  publication-title: Annu Rev Entomol
  doi: 10.1146/annurev.ento.52.110405.091434
  contributor:
    fullname: Y Le Conte
– volume: 25
  start-page: 881
  issue: 4
  year: 1999
  ident: 1336_CR17
  publication-title: J Chem Ecol
  doi: 10.1023/A:1020805103379
  contributor:
    fullname: G Bloch
– volume: 40
  start-page: 45
  year: 1998
  ident: 1336_CR54
  publication-title: Curr Top Dev Biol
  doi: 10.1016/S0070-2153(08)60364-6
  contributor:
    fullname: K Hartfelder
– volume-title: From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design
  year: 2005
  ident: 1336_CR50
  contributor:
    fullname: SB Carroll
– start-page: 195
  volume-title: Hormones, Brain and Behavior. Non-mammalian hormone-behavior systems
  year: 2002
  ident: 1336_CR19
  doi: 10.1016/B978-012532104-4/50042-1
  contributor:
    fullname: G Bloch
– volume-title: Insect Phylogeny
  year: 1981
  ident: 1336_CR71
  contributor:
    fullname: W Hennig
– volume: 322
  start-page: 896
  issue: 5903
  year: 2008
  ident: 1336_CR6
  publication-title: Science
  doi: 10.1126/science.1159277
  contributor:
    fullname: GE Robinson
– ident: 1336_CR20
  doi: 10.1007/BF00296638
– volume: 100
  start-page: 14519
  issue: Suppl 2
  year: 2003
  ident: 1336_CR32
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.2335884100
  contributor:
    fullname: CM Grozinger
– volume: 125
  start-page: 91
  year: 2008
  ident: 1336_CR46
  publication-title: Mech Dev
  doi: 10.1016/j.mod.2007.10.002
  contributor:
    fullname: C Minakuchi
– volume: 51
  start-page: 287
  year: 2004
  ident: 1336_CR14
  publication-title: Insect Sociaux
  doi: 10.1007/s00040-004-0741-5
  contributor:
    fullname: C Alaux
– volume: 51
  start-page: 811
  year: 2005
  ident: 1336_CR59
  publication-title: J Insect Physiol
  doi: 10.1016/j.jinsphys.2005.03.009
  contributor:
    fullname: S Geva
– volume-title: The Insect Societies
  year: 1971
  ident: 1336_CR2
  contributor:
    fullname: EO Wilson
– volume: 7
  start-page: 34
  year: 2009
  ident: 1336_CR37
  publication-title: BMC Biol
  doi: 10.1186/1741-7007-7-34
  contributor:
    fullname: BM Wiegmann
– volume: 107
  start-page: 186
  year: 1988
  ident: 1336_CR61
  publication-title: Behavior
  doi: 10.1163/156853988X00340
  contributor:
    fullname: MJ Duchateau
– volume: 95
  start-page: 515
  issue: 6
  year: 2008
  ident: 1336_CR18
  publication-title: Naturwissenschaften
  doi: 10.1007/s00114-008-0353-4
  contributor:
    fullname: A Sramkova
– volume: 83
  start-page: 626
  year: 1990
  ident: 1336_CR27
  publication-title: Ann Entomol Soc Am
  doi: 10.1093/aesa/83.3.626
  contributor:
    fullname: SA Cameron
– volume: 23
  start-page: 377
  issue: 7
  year: 2008
  ident: 1336_CR33
  publication-title: Trends in Ecology and Evolution
  doi: 10.1016/j.tree.2008.03.006
  contributor:
    fullname: GP Wagner
– volume: 94
  start-page: 375
  issue: 5
  year: 2007
  ident: 1336_CR30
  publication-title: Naturwissenschaften
  doi: 10.1007/s00114-006-0197-8
  contributor:
    fullname: CM Grozinger
– volume: 125
  start-page: 601
  year: 2008
  ident: 1336_CR48
  publication-title: Mech Dev
  doi: 10.1016/j.mod.2008.03.004
  contributor:
    fullname: R Parthasarathy
– volume: 16
  start-page: 4837
  issue: 22
  year: 2007
  ident: 1336_CR40
  publication-title: Mol Ecol
  doi: 10.1111/j.1365-294X.2007.03545.x
  contributor:
    fullname: CM Grozinger
– volume: 266
  start-page: 2465
  year: 1999
  ident: 1336_CR60
  publication-title: Proc R Soc Lond B Biol Sci
  doi: 10.1098/rspb.1999.0947
  contributor:
    fullname: G Bloch
– volume: 35
  start-page: 559
  issue: 4
  year: 1997
  ident: 1336_CR52
  publication-title: Arch Insect Biochem Physiol
  doi: 10.1002/(SICI)1520-6327(1997)35:4<559::AID-ARCH13>3.0.CO;2-9
  contributor:
    fullname: GE Robinson
– volume: 46
  start-page: 47
  issue: 1
  year: 2000
  ident: 1336_CR23
  publication-title: J Insect Physiol
  doi: 10.1016/S0022-1910(99)00101-8
  contributor:
    fullname: G Bloch
– volume: 57
  start-page: 141
  year: 2003
  ident: 1336_CR43
  publication-title: J Neurobiol
  doi: 10.1002/neu.10256
  contributor:
    fullname: SE Fahrbach
– volume: 58
  start-page: 625
  issue: 4
  year: 2001
  ident: 1336_CR35
  publication-title: Cell Mol Life Sci
  doi: 10.1007/PL00000885
  contributor:
    fullname: S Iuchi
– volume: 6
  start-page: 257
  issue: 4
  year: 2005
  ident: 1336_CR1
  publication-title: Nat Rev Genet
  doi: 10.1038/nrg1575
  contributor:
    fullname: GE Robinson
– volume: 186
  start-page: 261
  year: 2000
  ident: 1336_CR58
  publication-title: J Comp Physiol [A]
  doi: 10.1007/s003590050426
  contributor:
    fullname: G Bloch
– volume: 209
  start-page: 1044
  year: 2006
  ident: 1336_CR55
  publication-title: J Exp Biol
  doi: 10.1242/jeb.02125
  contributor:
    fullname: S Yerushalmi
– volume: 18
  start-page: 691
  issue: 5
  year: 2001
  ident: 1336_CR72
  publication-title: Mol Biol Evol
  doi: 10.1093/oxfordjournals.molbev.a003851
  contributor:
    fullname: S Whelan
– volume: 41
  start-page: 95
  year: 1999
  ident: 1336_CR64
  publication-title: Nucleo Acids Symp Ser
  contributor:
    fullname: TA Hall
– volume: 45
  start-page: 787
  year: 1993
  ident: 1336_CR5
  publication-title: Anim Beh
  doi: 10.1006/anbe.1993.1092
  contributor:
    fullname: L Keller
– start-page: 171
  volume-title: Effect of the queen on worker reproduction and new queen production in the bumble bee Bombus terrestris
  year: 2007
  ident: 1336_CR15
  contributor:
    fullname: C Lopez-Vaamonde
– volume: 51
  start-page: 199
  year: 1989
  ident: 1336_CR34
  publication-title: Entomol Exp Appl
  doi: 10.1111/j.1570-7458.1989.tb01231.x
  contributor:
    fullname: MJ Duchateau
– volume: 45
  start-page: 125
  year: 1999
  ident: 1336_CR38
  publication-title: Beh Ecol Sociobiol
  doi: 10.1007/s002650050546
  contributor:
    fullname: G Bloch
– volume: 52
  start-page: 696
  year: 2003
  ident: 1336_CR65
  publication-title: Syst Biol
  doi: 10.1080/10635150390235520
  contributor:
    fullname: S Guindon
– volume: 24
  start-page: 1596
  year: 2007
  ident: 1336_CR68
  publication-title: Mol Biol Evol
  doi: 10.1093/molbev/msm092
  contributor:
    fullname: K Tamura
– volume: 53
  start-page: 187
  year: 2007
  ident: 1336_CR63
  publication-title: J Insect Physiol
  doi: 10.1016/j.jinsphys.2006.11.009
  contributor:
    fullname: AB Barron
– volume: 8
  start-page: 275
  year: 1992
  ident: 1336_CR67
  publication-title: Comput Appl Biosci
  contributor:
    fullname: DT Jones
– start-page: 375
  volume-title: Orientation and Communication in Arthropods
  year: 1997
  ident: 1336_CR4
  doi: 10.1007/978-3-0348-8878-3_13
  contributor:
    fullname: R Gadagkar
– start-page: 1027
  volume-title: Hormones, Brain and Behavior
  year: 2009
  ident: 1336_CR29
  doi: 10.1016/B978-008088783-8.00030-9
  contributor:
    fullname: G Bloch
– volume: 29
  start-page: 305
  year: 2007
  ident: 1336_CR57
  publication-title: Entomologia Generalis
  doi: 10.1127/entom.gen/29/2007/305
  contributor:
    fullname: J Cnaani
– volume-title: The Social Behavior of Bees
  year: 1974
  ident: 1336_CR3
  contributor:
    fullname: CD Michener
– volume-title: Arthropod phylogeny with special reference to insects
  year: 1979
  ident: 1336_CR70
  contributor:
    fullname: HB Boudreaux
– volume: 14
  start-page: 211
  issue: 2
  year: 1989
  ident: 1336_CR26
  publication-title: Physiological Entomology
  doi: 10.1111/j.1365-3032.1989.tb00954.x
  contributor:
    fullname: A Van Doorn
– volume: 11
  start-page: 417
  issue: 6
  year: 2001
  ident: 1336_CR49
  publication-title: Curr Biol
  doi: 10.1016/S0960-9822(01)00124-5
  contributor:
    fullname: R Kraut
– volume: 179
  start-page: 314
  issue: 2
  year: 2007
  ident: 1336_CR9
  publication-title: Behav Brain Res
  doi: 10.1016/j.bbr.2007.02.014
  contributor:
    fullname: BC Trainor
– start-page: 290
  volume-title: Natural history and evolution of paper wasps
  year: 1996
  ident: 1336_CR53
  contributor:
    fullname: MJ West-Eberhard
– volume: 37
  start-page: 255
  issue: 3-4
  year: 1987
  ident: 1336_CR28
  publication-title: Netherland Journal of Zoology
  doi: 10.1163/002829687X00080
  contributor:
    fullname: A Van Doorn
– volume: 100
  start-page: 1
  year: 1949
  ident: 1336_CR39
  publication-title: Trans R Ent Soc Lond
  doi: 10.1111/j.1365-2311.1949.tb01420.x
  contributor:
    fullname: RA Cumber
– volume: 16
  start-page: 444
  year: 2001
  ident: 1336_CR56
  publication-title: J Biol Rhythms
  doi: 10.1177/074873001129002123
  contributor:
    fullname: G Bloch
– volume: 23
  start-page: 985
  year: 1977
  ident: 1336_CR25
  publication-title: J Insect Physiol
  doi: 10.1016/0022-1910(77)90126-3
  contributor:
    fullname: PF Roseler
– volume: 33
  start-page: 3
  year: 1986
  ident: 1336_CR62
  publication-title: Insect Sociaux
  doi: 10.1007/BF02224031
  contributor:
    fullname: A Van Doorn
– volume: 186
  start-page: 221
  issue: 3
  year: 2000
  ident: 1336_CR7
  publication-title: J Comp Physiol [A]
  doi: 10.1007/s003590050423
  contributor:
    fullname: EA Kravitz
– volume: 193
  start-page: 461
  issue: 4
  year: 2007
  ident: 1336_CR31
  publication-title: J Comp Physiol A Neuroethol Sens Neural Behav Physiol
  doi: 10.1007/s00359-006-0202-x
  contributor:
    fullname: CM Grozinger
– volume: 17
  start-page: 515
  year: 2008
  ident: 1336_CR42
  publication-title: Insect Mol Biol
  doi: 10.1111/j.1365-2583.2008.00819.x
  contributor:
    fullname: B Fussnecker
– volume: 60
  start-page: 439
  year: 2006
  ident: 1336_CR16
  publication-title: Behav Ecol Sociobiol
  doi: 10.1007/s00265-006-0184-2
  contributor:
    fullname: C Alaux
– volume: 23
  start-page: 334
  year: 2007
  ident: 1336_CR51
  publication-title: Trends Genet
  doi: 10.1016/j.tig.2007.05.001
  contributor:
    fullname: AL Toth
SSID ssj0017821
Score 1.9482332
Snippet Abstract Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and...
Background Regulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their...
SourceID proquest
crossref
SourceType Aggregation Database
StartPage 1
SubjectTerms Apis mellifera
Bees
Brain
Colonies
Division of labor
Down-regulation
Evolutionary conservation
Foraging behavior
Genomics
Homology
Honey
Hymenoptera
Insects
Juvenile hormones
Molecular modelling
Nurses
Nursing
Ovaries
Pheromones
Phylogeny
Physiology
Queen pheromone
Queenless
Social behavior
Social organization
Transcription factors
Workers (insect caste)
SummonAdditionalLinks – databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1LS8NAEF60IngRn1itsgcvHpZmt5vHnkTEUhQ9Wegt7CtY0CZt4sH_5s0_5kweai_ewoYl2RnmPbMfIZfRyHLjcOxDg7iBf2uZATYz4aRyJjCJDHHA-fEpmkzl_SyctQm3sm2r7HRirahdbjFHPhQK7w6LhVDXxZIhahRWV1sIjU2yxUUQYUtXPPsJuDhYP96VJpNoyEERM4EZtLojIVg3ReuauDYv4z2y2_qF9KZh5D7Z8IsDst0gRX7AUxvVHxIHjKUVWphO3mmDmUMfVl-fReFf6Uv-htson5cUC7Te0SqH1RWcwdN6VgT8TNqky2n-ZxqTzhfUeF8eken47vl2wlqoBGbRJjPjuDQmxBNr5Z0VSmuEE7M80CrLNLdK2cDKkXGh9hoiUxcHLkGBzmKXuNEx6S3gH04IlRY8QpklUksIzXimtRPGRjIzXkfwnT656qiWFs2NGGkdSSRRihROkcL1igj6ZNCRNW1lo0x_OXn6_-szstPU6rF2MyC9avXuz8EFqMxFzedvFQmx5A
  priority: 102
  providerName: ProQuest
Title The transcription factor Krüppel homolog 1is linked to hormone mediated social organization in bees
URI https://www.proquest.com/docview/2955187229
Volume 10
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LSwMxEA7aIngRn1itJQcvHlZ30-zrIGKlpSgWKRaKlyWvxUJt63YF-9-8-cecyXapBS9e9hBCdncmk5kvXyZDyHnQVJ7UmPYhwNwgvlWOBDU7TPNYS1dG3McE58de0B3w-6E_XKVHLwU4_xPaYT2pQTa-_Hxf3IDBX1uDj4IrDxZYh-HOmD1pAAC-yjjgdDzIx1ecAvhCC7_K3iVp-ccI605qfY22jqezS3aWESO9LVS8RzbMZJ9sFTUkFwdEg6Jpjh6ntH9a1NChD9n312xmxvR1-oadqTeaUyRsjab5FFozmIKG2twRiDtpsX1Op7-yM-loQqUx80My6LSf77rOsnSCo9BHO1J7XEof_1nERisWC4HlxZTnijhNhafiWLmKN6X2hRGAVHXo6ggNPA11pJtHpDKBbzgmlCuIEHkaccEBqnmpEJpJFfBUGhHAe2rkopRVMituyEgssoiCBOWaoFxtC3NrpF4KMylVnbAYb4ULGYtP_jHUKdkuiHwkduqkkmcf5gzig1w2yGY4DBuk2mr3nvoNi7IbdirAs996-QGOErrD
link.rule.ids 315,783,787,867,12068,21400,24330,27936,27937,31731,33756,43322,43817
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1LS8NAEF60RfQiPrFadQ9ePASz202anESlpdoHIi30FvYVLGgbm3jwv3nzjzmTh9qLt7BhSXaGee_MR8iF39JMGWz7kCBu4N9qRwGbHW5EaJSrAuFhg_Nw5Pcm4mHqTcuEW1peq6x0Yq6ozUJjjvyKhzg7rM15eJ28OYgahdXVEkJjndRxVBUEX_Xbzujx6aeOAPaPVcXJwL9ioIodjjm0_E6Cu2qMVnVxbmC6O2S79AzpTcHKXbJm53tko8CK_ICnMq7fJwZYSzO0MZXE0wI1h_aXX59JYl_o8-IVt1E2SymWaK2h2QJWl3AKS_NuEfA0aZEwp4s__Zh0NqfK2vSATLqd8V3PKcESHI1W2VGGCaU8PLEMrdE8lBIBxTRzZRjHkukw1K4WLWU8aSXEpqbtmgBFOm6bwLQOSW0O_3BEqNDgE4o4EFJAcMZiKQ1X2hexstKH7zTIZUW1KClmYkR5LBH4EVI4QgrnK9xtkGZF1qiUjjT65eXx_6_PyWZvPBxEg_tR_4RsFZV7rOQ0SS1bvttTcAgydVZy_RuuqLY6
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=The+transcription+factor+Kr%C3%BCppel+homolog+1is+linked+to+hormone+mediated+social+organization+in+bees&rft.jtitle=BMC+evolutionary+biology&rft.au=Shpigler%2C+Hagai&rft.au=Patch%2C+Harland+M&rft.au=Cohen%2C+Mira&rft.au=Fan%2C+Yongliang&rft.date=2010-04-30&rft.issn=1471-2148&rft.eissn=1471-2148&rft.volume=10&rft.issue=1&rft_id=info:doi/10.1186%2F1471-2148-10-120&rft.externalDBID=n%2Fa&rft.externalDocID=10_1186_1471_2148_10_120
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1471-2148&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1471-2148&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1471-2148&client=summon