Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance

Aqeel H. Al Jothery, Elzbieta Krol, James Hawkins, Aurore Chetoui, Alexander Saint-Lambert, Yuko Gamo, Suzanne C. Shaw, Teresa Valencak, Lutz Buenger, William G. Hill, Lobke M. Vaanholt, Catherine Hambly, John R. Speakman*

*Corresponding author for this work

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Maximal sustained energy intake (SusEI) appears limited, but the factors imposing the limit are disputed. We studied reproductive performance in two lines of mice selected for high and low food intake (MH and ML, respectively), and known to have large differences in thermal conductance (29% higher in the MH line at 21 degrees C). When these mice raised their natural litters, their metabolisable energy intake significantly increased over the first 13 days of lactation and then reached a plateau. At peak lactation, MH mice assimilated on average 45.3% more energy than ML mice (222.9 +/- 7.1 and 153.4 +/- 12.5 kJ day(-1), N=49 and 24, respectively). Moreover, MH mice exported on average 62.3 kJ day(-1) more energy as milk than ML mice (118.9 +/- 5.3 and 56.6 +/- 5.4 kJ day(-1), N=subset of 32 and 21, respectively). The elevated milk production of MH mice enabled them to wean litters (65.2 +/- 2.1 g) that were on average 50.2% heavier than litters produced by ML mothers (43.4 +/- 3.0 g), and pups that were on average 27.2% heavier (9.9 +/- 0.2 and 7.8 +/- 0.2 g, respectively). Lactating mice in both lines had significantly longer and heavier guts compared with non-reproductive mice. However, inconsistent with the 'central limit hypothesis', the ML mice had significantly longer and heavier intestines than MH mice. An experiment where the mice raised litters of the opposing line demonstrated that lactation performance was not limited by the growth capacity of offspring. Our findings are consistent with the idea that the SusEI at peak lactation is constrained by the capacity of the mothers to dissipate body heat.

Original languageEnglish
Pages (from-to)3718-3732
Number of pages15
JournalJournal of Experimental Biology
Volume217
Issue number20
Early online date11 Sep 2014
DOIs
Publication statusPublished - Oct 2014

Keywords

  • artificial selection
  • cross-fostering
  • daily energy expenditure
  • heat dissipation limit
  • milk production
  • lactation
  • doubly-labeled water
  • dissipation limitation hypothesis
  • resting metabolic-rate
  • voles lasiopodomys-brandtii
  • carbon-dioxide production
  • lactating European hares
  • mus-musculus
  • laboratory mice
  • food-intake
  • divergent selection

Cite this

Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance. / Al Jothery, Aqeel H.; Krol, Elzbieta; Hawkins, James; Chetoui, Aurore; Saint-Lambert, Alexander; Gamo, Yuko; Shaw, Suzanne C.; Valencak, Teresa; Buenger, Lutz; Hill, William G.; Vaanholt, Lobke M.; Hambly, Catherine; Speakman, John R.

In: Journal of Experimental Biology, Vol. 217, No. 20, 10.2014, p. 3718-3732.

Research output: Contribution to journalArticle

Al Jothery, AH, Krol, E, Hawkins, J, Chetoui, A, Saint-Lambert, A, Gamo, Y, Shaw, SC, Valencak, T, Buenger, L, Hill, WG, Vaanholt, LM, Hambly, C & Speakman, JR 2014, 'Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance', Journal of Experimental Biology, vol. 217, no. 20, pp. 3718-3732. https://doi.org/10.1242/jeb.103705
Al Jothery, Aqeel H. ; Krol, Elzbieta ; Hawkins, James ; Chetoui, Aurore ; Saint-Lambert, Alexander ; Gamo, Yuko ; Shaw, Suzanne C. ; Valencak, Teresa ; Buenger, Lutz ; Hill, William G. ; Vaanholt, Lobke M. ; Hambly, Catherine ; Speakman, John R. / Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance. In: Journal of Experimental Biology. 2014 ; Vol. 217, No. 20. pp. 3718-3732.
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abstract = "Maximal sustained energy intake (SusEI) appears limited, but the factors imposing the limit are disputed. We studied reproductive performance in two lines of mice selected for high and low food intake (MH and ML, respectively), and known to have large differences in thermal conductance (29{\%} higher in the MH line at 21 degrees C). When these mice raised their natural litters, their metabolisable energy intake significantly increased over the first 13 days of lactation and then reached a plateau. At peak lactation, MH mice assimilated on average 45.3{\%} more energy than ML mice (222.9 +/- 7.1 and 153.4 +/- 12.5 kJ day(-1), N=49 and 24, respectively). Moreover, MH mice exported on average 62.3 kJ day(-1) more energy as milk than ML mice (118.9 +/- 5.3 and 56.6 +/- 5.4 kJ day(-1), N=subset of 32 and 21, respectively). The elevated milk production of MH mice enabled them to wean litters (65.2 +/- 2.1 g) that were on average 50.2{\%} heavier than litters produced by ML mothers (43.4 +/- 3.0 g), and pups that were on average 27.2{\%} heavier (9.9 +/- 0.2 and 7.8 +/- 0.2 g, respectively). Lactating mice in both lines had significantly longer and heavier guts compared with non-reproductive mice. However, inconsistent with the 'central limit hypothesis', the ML mice had significantly longer and heavier intestines than MH mice. An experiment where the mice raised litters of the opposing line demonstrated that lactation performance was not limited by the growth capacity of offspring. Our findings are consistent with the idea that the SusEI at peak lactation is constrained by the capacity of the mothers to dissipate body heat.",
keywords = "artificial selection, cross-fostering, daily energy expenditure, heat dissipation limit, milk production, lactation, doubly-labeled water, dissipation limitation hypothesis, resting metabolic-rate, voles lasiopodomys-brandtii, carbon-dioxide production, lactating European hares, mus-musculus, laboratory mice, food-intake, divergent selection",
author = "{Al Jothery}, {Aqeel H.} and Elzbieta Krol and James Hawkins and Aurore Chetoui and Alexander Saint-Lambert and Yuko Gamo and Shaw, {Suzanne C.} and Teresa Valencak and Lutz Buenger and Hill, {William G.} and Vaanholt, {Lobke M.} and Catherine Hambly and Speakman, {John R.}",
note = "Acknowledgements We are grateful to the animal house staff who looked after the mice. Peter Thomson provided invaluable technical support for the isotope analysis. Funding The mice were selected under grants from BBSRC to W.G.H. and L.B., who was additionally supported by Cotswold International. A.H.A.J. was supported by a scholarship from the Iraqi government. A.C. and A.S.L. were supported by the Erasmus program and Y.G. was supported by a scholarship from the international rotary foundation. The work was also partly funded by research grants from NERC to J.R.S. and C.H. and from BBSRC to J.R.S. and E.K. J.R.S. was also supported by a 1000 Talents professorship during the final phase of the work.",
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T1 - Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance

AU - Al Jothery, Aqeel H.

AU - Krol, Elzbieta

AU - Hawkins, James

AU - Chetoui, Aurore

AU - Saint-Lambert, Alexander

AU - Gamo, Yuko

AU - Shaw, Suzanne C.

AU - Valencak, Teresa

AU - Buenger, Lutz

AU - Hill, William G.

AU - Vaanholt, Lobke M.

AU - Hambly, Catherine

AU - Speakman, John R.

N1 - Acknowledgements We are grateful to the animal house staff who looked after the mice. Peter Thomson provided invaluable technical support for the isotope analysis. Funding The mice were selected under grants from BBSRC to W.G.H. and L.B., who was additionally supported by Cotswold International. A.H.A.J. was supported by a scholarship from the Iraqi government. A.C. and A.S.L. were supported by the Erasmus program and Y.G. was supported by a scholarship from the international rotary foundation. The work was also partly funded by research grants from NERC to J.R.S. and C.H. and from BBSRC to J.R.S. and E.K. J.R.S. was also supported by a 1000 Talents professorship during the final phase of the work.

PY - 2014/10

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N2 - Maximal sustained energy intake (SusEI) appears limited, but the factors imposing the limit are disputed. We studied reproductive performance in two lines of mice selected for high and low food intake (MH and ML, respectively), and known to have large differences in thermal conductance (29% higher in the MH line at 21 degrees C). When these mice raised their natural litters, their metabolisable energy intake significantly increased over the first 13 days of lactation and then reached a plateau. At peak lactation, MH mice assimilated on average 45.3% more energy than ML mice (222.9 +/- 7.1 and 153.4 +/- 12.5 kJ day(-1), N=49 and 24, respectively). Moreover, MH mice exported on average 62.3 kJ day(-1) more energy as milk than ML mice (118.9 +/- 5.3 and 56.6 +/- 5.4 kJ day(-1), N=subset of 32 and 21, respectively). The elevated milk production of MH mice enabled them to wean litters (65.2 +/- 2.1 g) that were on average 50.2% heavier than litters produced by ML mothers (43.4 +/- 3.0 g), and pups that were on average 27.2% heavier (9.9 +/- 0.2 and 7.8 +/- 0.2 g, respectively). Lactating mice in both lines had significantly longer and heavier guts compared with non-reproductive mice. However, inconsistent with the 'central limit hypothesis', the ML mice had significantly longer and heavier intestines than MH mice. An experiment where the mice raised litters of the opposing line demonstrated that lactation performance was not limited by the growth capacity of offspring. Our findings are consistent with the idea that the SusEI at peak lactation is constrained by the capacity of the mothers to dissipate body heat.

AB - Maximal sustained energy intake (SusEI) appears limited, but the factors imposing the limit are disputed. We studied reproductive performance in two lines of mice selected for high and low food intake (MH and ML, respectively), and known to have large differences in thermal conductance (29% higher in the MH line at 21 degrees C). When these mice raised their natural litters, their metabolisable energy intake significantly increased over the first 13 days of lactation and then reached a plateau. At peak lactation, MH mice assimilated on average 45.3% more energy than ML mice (222.9 +/- 7.1 and 153.4 +/- 12.5 kJ day(-1), N=49 and 24, respectively). Moreover, MH mice exported on average 62.3 kJ day(-1) more energy as milk than ML mice (118.9 +/- 5.3 and 56.6 +/- 5.4 kJ day(-1), N=subset of 32 and 21, respectively). The elevated milk production of MH mice enabled them to wean litters (65.2 +/- 2.1 g) that were on average 50.2% heavier than litters produced by ML mothers (43.4 +/- 3.0 g), and pups that were on average 27.2% heavier (9.9 +/- 0.2 and 7.8 +/- 0.2 g, respectively). Lactating mice in both lines had significantly longer and heavier guts compared with non-reproductive mice. However, inconsistent with the 'central limit hypothesis', the ML mice had significantly longer and heavier intestines than MH mice. An experiment where the mice raised litters of the opposing line demonstrated that lactation performance was not limited by the growth capacity of offspring. Our findings are consistent with the idea that the SusEI at peak lactation is constrained by the capacity of the mothers to dissipate body heat.

KW - artificial selection

KW - cross-fostering

KW - daily energy expenditure

KW - heat dissipation limit

KW - milk production

KW - lactation

KW - doubly-labeled water

KW - dissipation limitation hypothesis

KW - resting metabolic-rate

KW - voles lasiopodomys-brandtii

KW - carbon-dioxide production

KW - lactating European hares

KW - mus-musculus

KW - laboratory mice

KW - food-intake

KW - divergent selection

U2 - 10.1242/jeb.103705

DO - 10.1242/jeb.103705

M3 - Article

VL - 217

SP - 3718

EP - 3732

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 20

ER -