Timing of Breeding Reveals a Trade-Off between Immune Investment and Life History in Tree Swallows

The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to dis...

Full description

Saved in:
Bibliographic Details
Published inIntegrative and comparative biology Vol. 62; no. 6; pp. 1629 - 1639
Main Authors Chang van Oordt, David A, Taff, Conor C, Ryan, Thomas A, Vitousek, Maren N
Format Journal Article
LanguageEnglish
Published England 30.12.2022
Subjects
Online AccessGet full text

Cover

Loading…
Abstract The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to disease. However, not all members of a population face identical constraints because differences in an individual's environmental context or physiological state can influence the degree to which traits are negatively associated. Here, we evaluated how variation in timing of breeding, a correlate of fitness, may result in different patterns of trait associations between immunity and reproduction. We measured constitutive immunity in breeding female tree swallows (Tachycineta bicolor) using a bacteria killing assay with blood plasma to assess the relationships between bacteria killing ability (BKA), reproductive effort, and reproductive success. We found that timing of breeding can influence the association between BKA and reproductive effort, but its effects are not homogeneous among all traits. Late-breeding tree swallows with stronger BKA laid smaller clutches, a pattern that was not apparent in early breeders. Regardless of the timing of breeding, birds with stronger BKA fed their nestlings less. Despite a negative association with reproductive effort, we found no association between immunity and reproductive success. We provide evidence that individual tree swallows do not experience some trade-offs equally, and that timing of breeding likely plays a role in how costs of immunity are weighed. To understand how investment in immunity can limit life history traits, we must consider how a variation among individuals influences the relative costs of immunity.
AbstractList Synopsis The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to disease. However, not all members of a population face identical constraints because differences in an individual's environmental context or physiological state can influence the degree to which traits are negatively associated. Here, we evaluated how variation in timing of breeding, a correlate of fitness, may result in different patterns of trait associations between immunity and reproduction. We measured constitutive immunity in breeding female tree swallows (Tachycineta bicolor) using a bacteria killing assay with blood plasma to assess the relationships between bacteria killing ability (BKA), reproductive effort, and reproductive success. We found that timing of breeding can influence the association between BKA and reproductive effort, but its effects are not homogeneous among all traits. Late-breeding tree swallows with stronger BKA laid smaller clutches, a pattern that was not apparent in early breeders. Regardless of the timing of breeding, birds with stronger BKA fed their nestlings less. Despite a negative association with reproductive effort, we found no association between immunity and reproductive success. We provide evidence that individual tree swallows do not experience some trade-offs equally, and that timing of breeding likely plays a role in how costs of immunity are weighed. To understand how investment in immunity can limit life history traits, we must consider how a variation among individuals influences the relative costs of immunity.
The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to disease. However, not all members of a population face identical constraints because differences in an individual's environmental context or physiological state can influence the degree to which traits are negatively associated. Here, we evaluated how variation in timing of breeding, a correlate of fitness, may result in different patterns of trait associations between immunity and reproduction. We measured constitutive immunity in breeding female tree swallows (Tachycineta bicolor) using a bacteria killing assay with blood plasma to assess the relationships between bacteria killing ability (BKA), reproductive effort, and reproductive success. We found that timing of breeding can influence the association between BKA and reproductive effort, but its effects are not homogeneous among all traits. Late-breeding tree swallows with stronger BKA laid smaller clutches, a pattern that was not apparent in early breeders. Regardless of the timing of breeding, birds with stronger BKA fed their nestlings less. Despite a negative association with reproductive effort, we found no association between immunity and reproductive success. We provide evidence that individual tree swallows do not experience some trade-offs equally, and that timing of breeding likely plays a role in how costs of immunity are weighed. To understand how investment in immunity can limit life history traits, we must consider how a variation among individuals influences the relative costs of immunity.
Author Taff, Conor C
Ryan, Thomas A
Chang van Oordt, David A
Vitousek, Maren N
Author_xml – sequence: 1
  givenname: David A
  orcidid: 0000-0001-6505-2299
  surname: Chang van Oordt
  fullname: Chang van Oordt, David A
  organization: Cornell Lab of Ornithology, Cornell University, 159 Sapsur ods Rd, Ithaca, NY 14850, USA
– sequence: 2
  givenname: Conor C
  orcidid: 0000-0003-1497-7990
  surname: Taff
  fullname: Taff, Conor C
  organization: Cornell Lab of Ornithology, Cornell University, 159 Sapsur ods Rd, Ithaca, NY 14850, USA
– sequence: 3
  givenname: Thomas A
  surname: Ryan
  fullname: Ryan, Thomas A
  organization: Cornell Lab of Ornithology, Cornell University, 159 Sapsur ods Rd, Ithaca, NY 14850, USA
– sequence: 4
  givenname: Maren N
  surname: Vitousek
  fullname: Vitousek, Maren N
  organization: Cornell Lab of Ornithology, Cornell University, 159 Sapsur ods Rd, Ithaca, NY 14850, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35561702$$D View this record in MEDLINE/PubMed
BookMark eNo9kF1LwzAUhoNM3IdeeS-5FKSajzZrL3VMNxgMdF6X0_RUIm06k3Zj_96MTS8OeSHPeTk8YzKwrUVCbjl75CyTT0YXYUAzKS_IiCfJNJoyIQfHHLOQlRySsfffjIVPxq_IUCaJ4gEakWJjGmO_aFvRF4dYHvM77hBqT4FuHJQYrauKFtjtES1dNk1vkS7tDn3XoO0o2JKuTIV0YXzXugM1Nuwh0o891HW799fksgp1eHN-J-Tzdb6ZLaLV-m05e15FWgrVRaA0KoVcCAUyYyXwpECZSKFT5FMeaw6YCGQZplJBClqoAkoRVwwhVpmSE3J_6t269qcP5-WN8RrrGiy2vc-FUnHKggQR0IcTql3rvcMq3zrTgDvknOVHqXmQmp-lBvruXNwXDZb_7J9F-Qs26HTh
CitedBy_id crossref_primary_10_1016_j_yhbeh_2024_105500
crossref_primary_10_3390_v15030703
crossref_primary_10_1242_jeb_247064
crossref_primary_10_1093_icb_icac148
Cites_doi 10.1098/rspb.2003.2424
10.1093/auk/121.2.345
10.1093/auk/105.4.706
10.1126/science.7123238
10.1111/j.1365-2656.2005.00950.x
10.1034/j.1600-0706.2000.880110.x
10.1016/j.ygcen.2007.04.007
10.1016/j.ygcen.2017.07.014
10.1111/j.1365-2435.2012.01997.x
10.1890/04-1619
10.1002/jez.2081
10.1086/665276
10.1146/annurev.ecolsys.36.102003.152622
10.1098/rstb.2007.2146
10.1111/j.1365-2435.2010.01759.x
10.4049/jimmunol.167.8.4543
10.1086/691059
10.1098/rsbl.2010.0531
10.1086/284547
10.1038/ni.3123
10.1016/j.mambio.2018.05.010
10.1093/icb/icr049
10.1007/s00114-010-0706-7
10.1098/rspb.2005.3376
10.1890/0012-9658(2001)082[2948:EOLHAE]2.0.CO;2
10.1086/518569
10.1093/auk/118.1.176
10.1073/pnas.2009864117
10.1016/0169-4758(96)80650-8
10.1016/S0169-5347(00)01941-8
10.1093/oxfordjournals.beheco.a000384
10.1111/j.1365-2435.2010.01777.x
10.1098/rsbl.2009.1078
10.1016/j.anbehav.2021.05.012
10.1002/ece3.504
10.1016/j.dci.2013.02.005
10.1642/AUK-13-020-R1.1
10.1111/j.1365-2435.2007.01311.x
10.1016/0169-5347(96)10039-2
10.1371/journal.pone.0230081
10.1016/j.dci.2006.05.013
10.1371/journal.pone.0049895
10.1086/501057
10.1016/j.tree.2012.04.008
10.1007/s00442-020-04618-8
10.1016/j.anbehav.2012.03.025
10.1093/auk/117.4.902
10.1098/rstb.1994.0149
10.1098/rspb.2018.0722
10.1016/j.anbehav.2004.05.005
10.1093/icb/icu082
10.2307/2265512
10.1093/beheco/11.1.19
10.1002/ecy.3109
10.1093/beheco/arl078
10.1111/j.0908-8857.2008.04408.x
10.1093/condor/106.4.768
ContentType Journal Article
Copyright The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.
Copyright_xml – notice: The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
DOI 10.1093/icb/icac033
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList CrossRef
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 fulltext_linktorsrc
Discipline Zoology
EISSN 1557-7023
EndPage 1639
ExternalDocumentID 10_1093_icb_icac033
35561702
Genre Research Support, U.S. Gov't, Non-P.H.S
Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
-DZ
-E4
-~X
.2P
.I3
0R~
18M
1TH
29J
2WC
4.4
482
48X
53G
5GY
5VS
5WA
5WD
70D
85S
AAHBH
AAHKG
AAIMJ
AAJKP
AAMDB
AAMVS
AAOGV
AAPQZ
AAPSS
AAPXW
AARHZ
AAUAY
AAVAP
AAVLN
ABEUO
ABIXL
ABJNI
ABLJU
ABMNT
ABNKS
ABPLY
ABPPZ
ABPTD
ABQLI
ABTLG
ABWST
ABXVV
ABZBJ
ACGFO
ACGFS
ACGOD
ACNCT
ACPRK
ACUFI
ADBBV
ADEYI
ADEZT
ADFTL
ADGKP
ADGZP
ADHKW
ADHZD
ADIPN
ADOCK
ADQBN
ADRIX
ADRTK
ADVEK
ADYVW
ADZTZ
ADZXQ
AEGPL
AEGXH
AEJOX
AEKSI
AELWJ
AEMDU
AENEX
AENZO
AEPUE
AETBJ
AEUPB
AEWNT
AFAZZ
AFFZL
AFGWE
AFIYH
AFOFC
AFRAH
AFXEN
AGINJ
AGKEF
AGQXC
AGSYK
AHXPO
AIAGR
AIJHB
AJEEA
AKWXX
ALMA_UNASSIGNED_HOLDINGS
ALUQC
APIBT
APWMN
ARIXL
ATGXG
AXUDD
AYOIW
BAWUL
BAYMD
BCRHZ
BEYMZ
BHONS
BQDIO
BSWAC
CDBKE
CGR
CS3
CUY
CVF
CZ4
DAKXR
DIK
DILTD
DU5
D~K
E3Z
EBS
ECGQY
ECM
EE~
EIF
ESX
F5P
F9B
FAC
FHSFR
FJW
FLUFQ
FOEOM
FQBLK
GAUVT
GJXCC
H13
H5~
HAR
HF~
HW0
HZ~
IOX
J21
JBS
JLS
JXSIZ
KAQDR
KOP
KQ8
KSI
KSN
M-Z
ML0
N9A
NGC
NLBLG
NOMLY
NPM
O9-
OAWHX
OBOKY
ODMLO
OJQWA
OJZSN
OK1
OWPYF
P2P
PAFKI
PEELM
PQ0
PQQKQ
Q1.
Q5Y
QN7
R44
RBO
RD5
RHF
ROL
ROX
RUSNO
RW1
RWL
RXO
TAE
TLC
TN5
TR2
UKR
UPT
W8F
WH7
WOQ
X7H
YAYTL
YKOAZ
YXANX
ZCA
ZKX
~02
~91
AASNB
AAYXX
CITATION
7X8
ID FETCH-LOGICAL-c326t-a6ce66e1226a390da15be3532c8e1714c1ae52e09e836a8ac26bad24f0ea46963
ISSN 1540-7063
IngestDate Sat Aug 17 03:35:44 EDT 2024
Fri Aug 23 01:09:28 EDT 2024
Wed Oct 16 00:40:31 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 6
Language English
License The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c326t-a6ce66e1226a390da15be3532c8e1714c1ae52e09e836a8ac26bad24f0ea46963
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0003-1497-7990
0000-0001-6505-2299
OpenAccessLink https://academic.oup.com/icb/article-pdf/62/6/1629/48448270/icac033.pdf
PMID 35561702
PQID 2664800012
PQPubID 23479
PageCount 11
ParticipantIDs proquest_miscellaneous_2664800012
crossref_primary_10_1093_icb_icac033
pubmed_primary_35561702
PublicationCentury 2000
PublicationDate 2022-12-30
PublicationDateYYYYMMDD 2022-12-30
PublicationDate_xml – month: 12
  year: 2022
  text: 2022-12-30
  day: 30
PublicationDecade 2020
PublicationPlace England
PublicationPlace_xml – name: England
PublicationTitle Integrative and comparative biology
PublicationTitleAlternate Integr Comp Biol
PublicationYear 2022
References Badyaev (2023051301055552000_bib7) 2001; 82
Sheldon (2023051301055552000_bib47) 1996; 11
French (2023051301055552000_bib17) 2007; 21
Hamilton (2023051301055552000_bib22) 1982; 218
MacColl (2023051301055552000_bib30) 2017; 327
Buehler (2023051301055552000_bib12) 2008; 39
Matson (2023051301055552000_bib33) 2006; 79
Adamo (2023051301055552000_bib1) 2004; 68
Graham (2023051301055552000_bib19) 2005; 36
Iwasaki (2023051301055552000_bib25) 2015; 16
Ardia (2023051301055552000_bib3) 2005; 74
McKean (2023051301055552000_bib35) 2005; 59
van Noordwijk (2023051301055552000_bib56) 1986; 128
Ruiz (2023051301055552000_bib45) 2011; 21
Williams (2023051301055552000_bib60) 1988; 105
Winkler (2023051301055552000_bib62) 2020; 101
McCarty (2023051301055552000_bib34) 2001; 118
Hasselquist (2023051301055552000_bib23) 2012; 83
Iseri (2023051301055552000_bib24) 2013; 40
Norris (2023051301055552000_bib39) 2000; 11
Shutler (2023051301055552000_bib49) 2011; 7
Matson (2023051301055552000_bib32) 2006; 273
Beechler (2023051301055552000_bib9) 2012; 85
Taff (2023051301055552000_bib52) 2021; 178
Murphy (2023051301055552000_bib38) 2000; 117
Twining (2023051301055552000_bib55) 2018; 56
Winkler (2023051301055552000_doi64_453_245222) 2004; 106
Ardia (2023051301055552000_bib5) 2011; 25
Millet (2023051301055552000_bib37) 2007; 31
French (2023051301055552000_bib16) 2007; 170
Verhulst (2023051301055552000_bib57) 2008; 363
Bartoń (2023051301055552000_bib8) 2020
Merrill (2023051301055552000_bib36) 2014; 131
Lochmiller (2023051301055552000_bib27) 2000; 88
Gustafsson (2023051301055552000_bib21) 1994; 346
Boyle (2023051301055552000_bib11) 2012; 26
Hasselquist (2023051301055552000_doi67_569_243422) 2001; 12
Bolker (2023051301055552000_bib66_1653420463349) 2020
Stearns (2023051301055552000_bib51) 1992
Roff (2023051301055552000_bib44) 1992
Love (2023051301055552000_bib28) 2017; 252
R Core Team (2023051301055552000_bib65_1653419231478) 2019
Ardia (2023051301055552000_bib2) 2005; 86
Ardia (2023051301055552000_bib6) 2003; 270
Cohen (2023051301055552000_bib13) 2012; 27
Shipley (2023051301055552000_bib48) 2020; 117
Keil (2023051301055552000_bib26) 2001; 167
Textor (2023051301055552000_bib53) 2017; 45
Ardia (2023051301055552000_bib4) 2007; 18
Graham (2023051301055552000_bib20) 2011; 25
Pigeon (2023051301055552000_bib41) 2013; 3
Trillmich (2023051301055552000_bib54) 2020; 15
Pyle (2023051301055552000_bib42) 1997
Bowlin (2023051301055552000_bib10) 2004; 121
Vitousek (2023051301055552000_bib58) 2018; 285
Cox (2023051301055552000_bib14) 2020; 192
Spence (2023051301055552000_bib50) 2017; 90
Martin (2023051301055552000_bib31) 2011; 51
Lucas (2023051301055552000_bib29) 2012; 7
Wilcoxen (2023051301055552000_bib59) 2010; 6
French (2023051301055552000_bib18) 2008; 155
Winkler (2023051301055552000_bib61) 1996; 77
Reznick (2023051301055552000_bib43) 2000; 15
Ruoss (2023051301055552000_bib46) 2019; 94
Downs (2023051301055552000_bib15) 2014; 54
Pap (2023051301055552000_bib40) 2010; 97
Zuk (2023051301055552000_bib63) 1996; 12
References_xml – volume: 270
  start-page: 1679
  year: 2003
  ident: 2023051301055552000_bib6
  article-title: Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolor)
  publication-title: Proc R Soc Lond B Biol Sci
  doi: 10.1098/rspb.2003.2424
  contributor:
    fullname: Ardia
– volume: 121
  start-page: 345
  year: 2004
  ident: 2023051301055552000_bib10
  article-title: Natural variation in flight performance is related to timing of breeding in tree swallows (Tachycineta bicolor) in New York
  publication-title: The Auk
  doi: 10.1093/auk/121.2.345
  contributor:
    fullname: Bowlin
– volume: 105
  start-page: 706
  year: 1988
  ident: 2023051301055552000_bib60
  article-title: Field metabolism of tree swallows during the breeding season
  publication-title: The Auk
  doi: 10.1093/auk/105.4.706
  contributor:
    fullname: Williams
– volume: 218
  start-page: 384
  year: 1982
  ident: 2023051301055552000_bib22
  article-title: Heritable true fitness and bright birds: a role for parasites?
  publication-title: Science
  doi: 10.1126/science.7123238
  contributor:
    fullname: Hamilton
– volume: 74
  start-page: 517
  year: 2005
  ident: 2023051301055552000_bib3
  article-title: Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows
  publication-title: J Anim Ecol
  doi: 10.1111/j.1365-2656.2005.00950.x
  contributor:
    fullname: Ardia
– volume: 88
  start-page: 87
  year: 2000
  ident: 2023051301055552000_bib27
  article-title: Trade-offs in evolutionary immunology: just what is the cost of immunity?
  publication-title: Oikos
  doi: 10.1034/j.1600-0706.2000.880110.x
  contributor:
    fullname: Lochmiller
– volume: 155
  start-page: 148
  year: 2008
  ident: 2023051301055552000_bib18
  article-title: Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus
  publication-title: Gen Comp Endocrinol
  doi: 10.1016/j.ygcen.2007.04.007
  contributor:
    fullname: French
– volume: 252
  start-page: 18
  year: 2017
  ident: 2023051301055552000_bib28
  article-title: Captivity influences immune responses, stress endocrinology, and organ size in house sparrows (Passer domesticus)
  publication-title: Gen Comp Endocrinol
  doi: 10.1016/j.ygcen.2017.07.014
  contributor:
    fullname: Love
– year: 2019
  ident: 2023051301055552000_bib65_1653419231478
  article-title: R: A language and environment for statistical computing
  contributor:
    fullname: R Core Team
– volume: 26
  start-page: 895
  year: 2012
  ident: 2023051301055552000_bib11
  article-title: Rapid loss of fat but not lean mass prior to chick provisioning supports the flight efficiency hypothesis in tree swallows
  publication-title: Funct Ecol
  doi: 10.1111/j.1365-2435.2012.01997.x
  contributor:
    fullname: Boyle
– volume: 45
  start-page: 1887
  year: 2017
  ident: 2023051301055552000_bib53
  article-title: Robust causal inference using directed acyclic graphs: the R package “dagitty
  publication-title: Int J Epidemiol
  contributor:
    fullname: Textor
– volume: 56
  start-page: 515
  year: 2018
  ident: 2023051301055552000_bib55
  article-title: Aquatic insects rich in omega-3 fatty acids drive breeding success in a widespread bird
  publication-title: Ecol Lett
  contributor:
    fullname: Twining
– volume: 86
  start-page: 2040
  year: 2005
  ident: 2023051301055552000_bib2
  article-title: Tree swallows trade off immune function and reproductive effort differently across their range
  publication-title: Ecology
  doi: 10.1890/04-1619
  contributor:
    fullname: Ardia
– volume: 327
  start-page: 243
  year: 2017
  ident: 2023051301055552000_bib30
  article-title: Correlates of immune defenses in golden eagle nestlings
  publication-title: J Exp Zool Part Ecol Integr Physiol
  doi: 10.1002/jez.2081
  contributor:
    fullname: MacColl
– volume: 85
  start-page: 255
  year: 2012
  ident: 2023051301055552000_bib9
  article-title: Innate immunity in free-ranging African buffalo(Syncerus caffer): associations with parasite infection and white blood cell counts
  publication-title: Physiol Biochem Zool
  doi: 10.1086/665276
  contributor:
    fullname: Beechler
– volume: 36
  start-page: 373
  year: 2005
  ident: 2023051301055552000_bib19
  article-title: Evolutionary causes and consequences of immunopathology
  publication-title: Annu Rev Ecol Evol Syst
  doi: 10.1146/annurev.ecolsys.36.102003.152622
  contributor:
    fullname: Graham
– volume: 363
  start-page: 399
  year: 2008
  ident: 2023051301055552000_bib57
  article-title: The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding
  publication-title: Philos Trans R Soc B Biol Sci
  doi: 10.1098/rstb.2007.2146
  contributor:
    fullname: Verhulst
– volume: 25
  start-page: 61
  year: 2011
  ident: 2023051301055552000_bib5
  article-title: The role of constraints and limitation in driving individual variation in immune response
  publication-title: Funct Ecol
  doi: 10.1111/j.1365-2435.2010.01759.x
  contributor:
    fullname: Ardia
– volume: 167
  start-page: 4543
  year: 2001
  ident: 2023051301055552000_bib26
  article-title: Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism
  publication-title: J Immunol
  doi: 10.4049/jimmunol.167.8.4543
  contributor:
    fullname: Keil
– volume: 90
  start-page: 321
  year: 2017
  ident: 2023051301055552000_bib50
  article-title: Physiological correlates of multiple parasitic infections in side-blotched lizards
  publication-title: Physiol Biochem Zool
  doi: 10.1086/691059
  contributor:
    fullname: Spence
– volume-title: Identification guide to North American birds
  year: 1997
  ident: 2023051301055552000_bib42
  contributor:
    fullname: Pyle
– volume-title: The evolution of life histories Oxford
  year: 1992
  ident: 2023051301055552000_bib51
  contributor:
    fullname: Stearns
– volume: 7
  start-page: 101
  year: 2011
  ident: 2023051301055552000_bib49
  article-title: Sexual selection: when to expect trade-offs
  publication-title: Biol Lett
  doi: 10.1098/rsbl.2010.0531
  contributor:
    fullname: Shutler
– volume: 128
  start-page: 137
  year: 1986
  ident: 2023051301055552000_bib56
  article-title: Acquisition and allocation of resources: their influence on variation in life history tactics
  publication-title: Am Nat
  doi: 10.1086/284547
  contributor:
    fullname: van Noordwijk
– year: 2020
  ident: 2023051301055552000_bib8
  article-title: MuMIn: multi-model inference
  contributor:
    fullname: Bartoń
– year: 2020
  ident: 2023051301055552000_bib66_1653420463349
  article-title: bbmle: Tools for general maximum likelihood estimation
  contributor:
    fullname: Bolker
– volume: 16
  start-page: 343
  year: 2015
  ident: 2023051301055552000_bib25
  article-title: Control of adaptive immunity by the innate immune system
  publication-title: Nat Immunol
  doi: 10.1038/ni.3123
  contributor:
    fullname: Iwasaki
– volume: 94
  start-page: 120
  year: 2019
  ident: 2023051301055552000_bib46
  article-title: Effect of sex and reproductive status on the immunity of the temperate bat Myotis daubentonii
  publication-title: Mamm Biol
  doi: 10.1016/j.mambio.2018.05.010
  contributor:
    fullname: Ruoss
– volume: 51
  start-page: 514
  year: 2011
  ident: 2023051301055552000_bib31
  article-title: Integrator networks: illuminating the black box linking genotype and phenotype
  publication-title: Integr Comp Biol
  doi: 10.1093/icb/icr049
  contributor:
    fullname: Martin
– volume: 97
  start-page: 891
  year: 2010
  ident: 2023051301055552000_bib40
  article-title: Sexual dimorphism in immune function changes during the annual cycle in house sparrows
  publication-title: Naturwissenschaften
  doi: 10.1007/s00114-010-0706-7
  contributor:
    fullname: Pap
– volume: 273
  start-page: 815
  year: 2006
  ident: 2023051301055552000_bib32
  article-title: No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl
  publication-title: Proc R Soc B Biol Sci
  doi: 10.1098/rspb.2005.3376
  contributor:
    fullname: Matson
– volume: 82
  start-page: 2948
  year: 2001
  ident: 2023051301055552000_bib7
  article-title: Evolution of life histories along elevational gradients: trade-off between parental care and fecundity
  publication-title: Ecology
  doi: 10.1890/0012-9658(2001)082[2948:EOLHAE]2.0.CO;2
  contributor:
    fullname: Badyaev
– volume: 170
  start-page: 79
  year: 2007
  ident: 2023051301055552000_bib16
  article-title: Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction?
  publication-title: Am Nat
  doi: 10.1086/518569
  contributor:
    fullname: French
– volume: 118
  start-page: 176
  year: 2001
  ident: 2023051301055552000_bib34
  article-title: Variation in growth of nestling tree swallows across multiple temporal and spatial scales
  publication-title: The Auk
  doi: 10.1093/auk/118.1.176
  contributor:
    fullname: McCarty
– volume: 117
  start-page: 25590
  year: 2020
  ident: 2023051301055552000_bib48
  article-title: Birds advancing lay dates with warming springs face greater risk of chick mortality
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.2009864117
  contributor:
    fullname: Shipley
– volume: 12
  start-page: 46
  year: 1996
  ident: 2023051301055552000_bib63
  article-title: Trade-offs in parasitology, evolution and behavior
  publication-title: Parasitol Today
  doi: 10.1016/0169-4758(96)80650-8
  contributor:
    fullname: Zuk
– volume: 15
  start-page: 421
  year: 2000
  ident: 2023051301055552000_bib43
  article-title: Big houses, big cars, superfleas and the costs of reproduction
  publication-title: Trends Ecol Evol
  doi: 10.1016/S0169-5347(00)01941-8
  contributor:
    fullname: Reznick
– volume: 12
  start-page: 93
  year: 2001
  ident: 2023051301055552000_doi67_569_243422
  article-title: Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows
  publication-title: Behavioral Ecology
  doi: 10.1093/oxfordjournals.beheco.a000384
  contributor:
    fullname: Hasselquist
– volume: 25
  start-page: 5
  year: 2011
  ident: 2023051301055552000_bib20
  article-title: Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology
  publication-title: Funct Ecol
  doi: 10.1111/j.1365-2435.2010.01777.x
  contributor:
    fullname: Graham
– volume: 6
  start-page: 552
  year: 2010
  ident: 2023051301055552000_bib59
  article-title: Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic
  publication-title: Biol Lett
  doi: 10.1098/rsbl.2009.1078
  contributor:
    fullname: Wilcoxen
– volume: 178
  start-page: 11
  year: 2021
  ident: 2023051301055552000_bib52
  article-title: Plumage manipulation alters associations between behaviour, physiology, the internal microbiome and fitness
  publication-title: Anim Behav
  doi: 10.1016/j.anbehav.2021.05.012
  contributor:
    fullname: Taff
– volume: 3
  start-page: 1091
  year: 2013
  ident: 2023051301055552000_bib41
  article-title: Ecological immunology in a fluctuating environment: an integrative analysis of tree swallow nestling immune defense
  publication-title: Ecol Evol
  doi: 10.1002/ece3.504
  contributor:
    fullname: Pigeon
– volume: 40
  start-page: 248
  year: 2013
  ident: 2023051301055552000_bib24
  article-title: Dynamics of the systemic components of the chicken (Gallus gallus domesticus) immune system following activation by Escherichia coli; implications for the costs of immunity
  publication-title: Dev Comp Immunol
  doi: 10.1016/j.dci.2013.02.005
  contributor:
    fullname: Iseri
– volume: 131
  start-page: 3
  year: 2014
  ident: 2023051301055552000_bib36
  article-title: Bacteria-killing ability is negatively linked to epaulet size, but positively linked to baseline corticosterone, in male red-winged blackbirds (Agelaius phoeniceus)
  publication-title: The Auk
  doi: 10.1642/AUK-13-020-R1.1
  contributor:
    fullname: Merrill
– volume: 59
  start-page: 1510
  year: 2005
  ident: 2023051301055552000_bib35
  article-title: Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences
  publication-title: Evolution
  contributor:
    fullname: McKean
– volume: 21
  start-page: 131
  year: 2011
  ident: 2023051301055552000_bib45
  article-title: Trade-offs between reproductive coloration and innate immunity in a natural population of female sagebrush lizards, Sceloporus graciosus
  publication-title: Herp J
  contributor:
    fullname: Ruiz
– volume: 21
  start-page: 1115
  year: 2007
  ident: 2023051301055552000_bib17
  article-title: Immune activity suppresses reproduction in food-limited female tree lizards Urosaurus ornatus
  publication-title: Funct Ecol
  doi: 10.1111/j.1365-2435.2007.01311.x
  contributor:
    fullname: French
– volume: 11
  start-page: 317
  year: 1996
  ident: 2023051301055552000_bib47
  article-title: Ecological immunology—costly parasite defenses and trade-offs in evolutionary ecology
  publication-title: Trends Ecol Evol
  doi: 10.1016/0169-5347(96)10039-2
  contributor:
    fullname: Sheldon
– volume-title: The evolution of life histories: theory and analysis
  year: 1992
  ident: 2023051301055552000_bib44
  contributor:
    fullname: Roff
– volume: 15
  start-page: e0230081
  year: 2020
  ident: 2023051301055552000_bib54
  article-title: Reproduction affects immune defenses in the guinea pig even under ad libitum food
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0230081
  contributor:
    fullname: Trillmich
– volume: 31
  start-page: 188
  year: 2007
  ident: 2023051301055552000_bib37
  article-title: Quantifying and comparing constitutive immunity across avian species
  publication-title: Dev Comp Immunol
  doi: 10.1016/j.dci.2006.05.013
  contributor:
    fullname: Millet
– volume: 7
  start-page: e49895
  year: 2012
  ident: 2023051301055552000_bib29
  article-title: Stress-induced tradeoffs in a free-living lizard across a variable landscape: consequences for individuals and populations
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0049895
  contributor:
    fullname: Lucas
– volume: 79
  start-page: 5 56
  year: 2006
  ident: 2023051301055552000_bib33
  article-title: Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds
  publication-title: Physiol Biochem Zool
  doi: 10.1086/501057
  contributor:
    fullname: Matson
– volume: 27
  start-page: 428
  year: 2012
  ident: 2023051301055552000_bib13
  article-title: Physiological regulatory networks: ecological roles and evolutionary constraints
  publication-title: Trends Ecol Evol
  doi: 10.1016/j.tree.2012.04.008
  contributor:
    fullname: Cohen
– volume: 192
  start-page: 713
  year: 2020
  ident: 2023051301055552000_bib14
  article-title: Population decline in tree swallows (Tachycineta bicolor) linked to climate change and inclement weather on the breeding ground
  publication-title: Oecologia
  doi: 10.1007/s00442-020-04618-8
  contributor:
    fullname: Cox
– volume: 83
  start-page: 1303
  year: 2012
  ident: 2023051301055552000_bib23
  article-title: Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds?
  publication-title: Anim Behav
  doi: 10.1016/j.anbehav.2012.03.025
  contributor:
    fullname: Hasselquist
– volume: 117
  start-page: 902
  year: 2000
  ident: 2023051301055552000_bib38
  article-title: Is reproduction by tree swallows cost free?
  publication-title: The Auk
  doi: 10.1093/auk/117.4.902
  contributor:
    fullname: Murphy
– volume: 346
  start-page: 323
  year: 1994
  ident: 2023051301055552000_bib21
  article-title: Infectious diseases, reproductive effort and the cost of reproduction in birds
  publication-title: Philos Trans R Soc Lond B Biol Sci
  doi: 10.1098/rstb.1994.0149
  contributor:
    fullname: Gustafsson
– volume: 285
  start-page: 20180722
  year: 2018
  ident: 2023051301055552000_bib58
  article-title: The lingering impact of stress: brief acute glucocorticoid exposure has sustained, dose-dependent effects on reproduction
  publication-title: Proc R Soc B Biol Sci
  doi: 10.1098/rspb.2018.0722
  contributor:
    fullname: Vitousek
– volume: 68
  start-page: 1443
  year: 2004
  ident: 2023051301055552000_bib1
  article-title: How should behavioural ecologists interpret measurements of immunity?
  publication-title: Anim Behav
  doi: 10.1016/j.anbehav.2004.05.005
  contributor:
    fullname: Adamo
– volume: 54
  start-page: 340
  year: 2014
  ident: 2023051301055552000_bib15
  article-title: Mechanisms and methods in ecoimmunology: integrating within-organism and between-organism processes
  publication-title: Integr Comp Biol
  doi: 10.1093/icb/icu082
  contributor:
    fullname: Downs
– volume: 77
  start-page: 922
  year: 1996
  ident: 2023051301055552000_bib61
  article-title: The seasonal decline in tree swallow clutch size: physiological constraint or strategic adjustment?
  publication-title: Ecology
  doi: 10.2307/2265512
  contributor:
    fullname: Winkler
– volume: 11
  start-page: 19
  year: 2000
  ident: 2023051301055552000_bib39
  article-title: Ecological immunology: life history trade-offs and immune defense in birds
  publication-title: Behav Ecol
  doi: 10.1093/beheco/11.1.19
  contributor:
    fullname: Norris
– volume: 101
  start-page: 1
  year: 2020
  ident: 2023051301055552000_bib62
  article-title: Full lifetime perspectives on the costs and benefits of lay-date variation in tree swallows
  publication-title: Ecology
  doi: 10.1002/ecy.3109
  contributor:
    fullname: Winkler
– volume: 18
  start-page: 259
  year: 2007
  ident: 2023051301055552000_bib4
  article-title: Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird
  publication-title: Behav Ecol
  doi: 10.1093/beheco/arl078
  contributor:
    fullname: Ardia
– volume: 39
  start-page: 560
  year: 2008
  ident: 2023051301055552000_bib12
  article-title: Captive and free-living red knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments
  publication-title: J Avian Biol
  doi: 10.1111/j.0908-8857.2008.04408.x
  contributor:
    fullname: Buehler
– volume: 106
  start-page: 768
  year: 2004
  ident: 2023051301055552000_doi64_453_245222
  article-title: Breeding Dispersal and Philopatry in the Tree Swallow
  publication-title: The Condor
  doi: 10.1093/condor/106.4.768
  contributor:
    fullname: Winkler
SSID ssj0015501
Score 2.4401226
Snippet The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the...
Synopsis The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In...
SourceID proquest
crossref
pubmed
SourceType Aggregation Database
Index Database
StartPage 1629
SubjectTerms Animals
Life History Traits
Reproduction
Swallows - physiology
Title Timing of Breeding Reveals a Trade-Off between Immune Investment and Life History in Tree Swallows
URI https://www.ncbi.nlm.nih.gov/pubmed/35561702
https://search.proquest.com/docview/2664800012
Volume 62
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELaWIlAviDfLS0bqDYXGTuI4RyiglkcrwRZVXCLbGaOlarZaUiE48NsZP_JAUAk4bLRKdu2sv28n4_HMZ0K2lLSNkYwl0rrQTYN_Kc01ApJpA1aW0PhkzLf7Yvcwf3VUHM1mP6bVJZ1-Yr7_sa7kf1DFc4irq5L9B2SHRvEEvkd88YgI4_HvMHZbcvmk5Wfr8BRysX5wisjKyZY3kBxYO-Ri7blaEIjSGkNy-ZulhagW4msAF9jU4_df3YJ8dLg_j9nun6JQeKyGG4TDo5bTJFkA78WVRh3g5LYbkufHyOlCBTnInVW7Wo-h2nff4nbJPm9p_PgHNDxnX-A4lhfhj9mfxiu43zolLr1AtLFFmZRpKDPujbDgE7JNLSoTISLym6kPMlhLo_1RmTQIakxgPz3xuGduB9Ay5eMTb8hD7C9dIBd5WRUuJfT53uthFQpnbyzWdGJv29jXduxpk1zuv_urQ3POLMV7K4ur5EqcZtCngTPXyAza6-TSx5VH6QbRgTl0ZWnPHBqZQxUdmEMjc2hgDh2ZQ5EA1DGHRubQZUsdc2jPnJvk8OWLxc5uEnfbSAy68F2ihAEhgKE_rrIqbRQrNGRFxo0EVrLcMAUFh7QCmQklleFCq4bnNgWVC7Tjt8hGu2rhDqEgVSaq3NqqNHnFrc5A48vIhnn9pDnZ6oesPg2iKnVIhshqHOQ6DvKcPOqHs0aj51ayVAvIthq9ylz6IOqc3A7jPDTU43L33Cv3yOZIzPtko1ufwQN0LTv90OP_E2adfF4
link.rule.ids 315,786,790,27955,27956
linkProvider Flying Publisher
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=Timing+of+Breeding+Reveals+a+Trade-Off+between+Immune+Investment+and+Life+History+in+Tree+Swallows&rft.jtitle=Integrative+and+comparative+biology&rft.au=Chang+van+Oordt%2C+David+A&rft.au=Taff%2C+Conor+C&rft.au=Ryan%2C+Thomas+A&rft.au=Vitousek%2C+Maren+N&rft.date=2022-12-30&rft.eissn=1557-7023&rft.volume=62&rft.issue=6&rft.spage=1629&rft_id=info:doi/10.1093%2Ficb%2Ficac033&rft_id=info%3Apmid%2F35561702&rft.externalDocID=35561702
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1540-7063&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1540-7063&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1540-7063&client=summon