Greater male variability in daily energy expenditure develops through puberty

Lewis G. Halsey; Vincent Careau; Philip N. Ainslie; Heliodoro Alemán-Mateo; Lene F. Andersen; Liam J. Anderson; Leonore Arab; Issad Baddou; Linda Bandini; Kweku Bedu-Addo; Ellen E. Blaak; Stephane Blanc; Alberto G. Bonomi; Carlijn V. C. Bouten; Pascal Bovet; Soren Brage; Maciej S. Buchowski; Nancy F. Butte; Stephan G. Camps; Regina Casper; Graeme L. Close; Lisa H. Colbert; Jamie A. Cooper; Richard Cooper; Prasangi Dabare; Sai Krupa Das; Peter S. W. Davies; Sanjoy Deb; Christine Delisle Nyström; William Dietz; Lara R. Dugas; Simon Eaton; Ulf Ekelund; Asmaa El Hamdouchi; Sonja Entringer; Terrence Forrester; Barry W. Fudge; Melanie Gillingham; Annelies H. Goris; Michael Gurven; Hinke Haisma; Catherine Hambly; Daniel J. Hoffman; Marije B. Hoos; Sumei Hu; Noorjehan Joonas; Annemiek Joosen; Peter Katzmarzyk; Kitty P. Kempen; Misaka Kimura; William E. Kraus; Wantanee Kriengsinyos; Rebecca Kuriyan; Robert F. Kushner; Estelle V. Lambert; Pulani Lanerolle; Christel L. Larsson; Nader Lessan; Marie Löf; Corby K. Martin; Eric Matsiko; Gerwin A. Meijer; James C. Morehen; James P. Morton; Aviva Must; Marian Neuhouser; Theresa A. Nicklas; Robert M. Ojiambo; Kirsi H. Pietilainen; Yannis P. Pitsiladis; Jacob Plange-Rhule; Guy Plasqui; Ross L. Prentice; Roberto Rabinovich; Susan B. Racette; David A. Raichen; Eric Ravussin; Leanne Redman; John J. Reilly; Rebecca M. Reynolds; Susan Roberts; Dulani Samaranayake; Luís B. Sardinha; Albertine J. Schuit; Analiza M. Silva; Srishti Sinha; Anders M. Sjödin; Eric Stice; Albert Stunkard; Samuel S. Urlacher; Mauro Eduardo Valencia; Giulio Valenti; Ludo M. van Etten; Edgar A. Van Mil; Jeanine A. Verbunt; Jonathan C. K. Wells; George Wilson; Brian Wood; Tsukasa Yoshida; Xueying Zhang; Alexia Murphy-Alford; Cornelia Loechl; Amy Luke; Herman Pontzer; Jennifer Rood; Hiroyuki Sagayama; Klaas R. Westerterp; William W. Wong; Yosuke Yamada; John R. Speakman; IAEA DLW Database Consortium

doi:10.1098/rsbl.2023.0152

Greater male variability in daily energy expenditure develops through puberty

Lewis G. Halsey^*, Vincent Careau, Philip N. Ainslie, Heliodoro Alemán-Mateo, Lene F. Andersen, Liam J. Anderson, Leonore Arab, Issad Baddou, Linda Bandini, Kweku Bedu-Addo, Ellen E. Blaak, Stephane Blanc, Alberto G. Bonomi, Carlijn V. C. Bouten, Pascal Bovet, Soren Brage, Maciej S. Buchowski, Nancy F. Butte, Stephan G. Camps, Regina CasperGraeme L. Close, Lisa H. Colbert, Jamie A. Cooper, Richard Cooper, Prasangi Dabare, Sai Krupa Das, Peter S. W. Davies, Sanjoy Deb, Christine Delisle Nyström, William Dietz, Lara R. Dugas, Simon Eaton, Ulf Ekelund, Asmaa El Hamdouchi, Sonja Entringer, Terrence Forrester, Barry W. Fudge, Melanie Gillingham, Annelies H. Goris, Michael Gurven, Hinke Haisma, Catherine Hambly, Daniel J. Hoffman, Marije B. Hoos, Sumei Hu, Noorjehan Joonas, Annemiek Joosen, Peter Katzmarzyk, Kitty P. Kempen, Misaka Kimura, William E. Kraus, Wantanee Kriengsinyos, Rebecca Kuriyan, Robert F. Kushner, Estelle V. Lambert, Pulani Lanerolle, Christel L. Larsson, Nader Lessan, Marie Löf, Corby K. Martin, Eric Matsiko, Gerwin A. Meijer, James C. Morehen, James P. Morton, Aviva Must, Marian Neuhouser, Theresa A. Nicklas, Robert M. Ojiambo, Kirsi H. Pietilainen, Yannis P. Pitsiladis, Jacob Plange-Rhule, Guy Plasqui, Ross L. Prentice, Roberto Rabinovich, Susan B. Racette, David A. Raichen, Eric Ravussin, Leanne Redman, John J. Reilly, Rebecca M. Reynolds, Susan Roberts, Dulani Samaranayake, Luís B. Sardinha, Albertine J. Schuit, Analiza M. Silva, Srishti Sinha, Anders M. Sjödin, Eric Stice, Albert Stunkard, Samuel S. Urlacher, Mauro Eduardo Valencia, Giulio Valenti, Ludo M. van Etten, Edgar A. Van Mil, Jeanine A. Verbunt, Jonathan C. K. Wells, George Wilson, Brian Wood, Tsukasa Yoshida, Xueying Zhang, Alexia Murphy-Alford^*, Cornelia Loechl^*, Amy Luke^*, Herman Pontzer^*, Jennifer Rood^*, Hiroyuki Sagayama^*, Klaas R. Westerterp^*, William W. Wong^*, Yosuke Yamada^*, John R. Speakman^*, IAEA DLW Database Consortium

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › peer-review

Abstract

There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decrease in the degree of GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

Original language	English
Article number	20230152
Number of pages	5
Journal	Biology Letters
Volume	19
Issue number	9
DOIs	https://doi.org/10.1098/rsbl.2023.0152
Publication status	Published - 20 Sept 2023

Scopus Subject Areas

Agricultural and Biological Sciences (miscellaneous)
General Agricultural and Biological Sciences

User-Defined Keywords

age
height
inter-individual variation
morphometry
weight

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1098/rsbl.2023.0152

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Halsey, L. G., Careau, V., Ainslie, P. N., Alemán-Mateo, H., Andersen, L. F., Anderson, L. J., Arab, L., Baddou, I., Bandini, L., Bedu-Addo, K., Blaak, E. E., Blanc, S., Bonomi, A. G., Bouten, C. V. C., Bovet, P., Brage, S., Buchowski, M. S., Butte, N. F., Camps, S. G., ... IAEA DLW Database Consortium (2023). Greater male variability in daily energy expenditure develops through puberty. Biology Letters, 19(9), Article 20230152. https://doi.org/10.1098/rsbl.2023.0152

@article{a2b0985eaa1143ba910d8f93e8b8a5da,

title = "Greater male variability in daily energy expenditure develops through puberty",

abstract = "There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decrease in the degree of GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.",

keywords = "age, height, inter-individual variation, morphometry, weight",

author = "Halsey, {Lewis G.} and Vincent Careau and Ainslie, {Philip N.} and Heliodoro Alem{\'a}n-Mateo and Andersen, {Lene F.} and Anderson, {Liam J.} and Leonore Arab and Issad Baddou and Linda Bandini and Kweku Bedu-Addo and Blaak, {Ellen E.} and Stephane Blanc and Bonomi, {Alberto G.} and Bouten, {Carlijn V. C.} and Pascal Bovet and Soren Brage and Buchowski, {Maciej S.} and Butte, {Nancy F.} and Camps, {Stephan G.} and Regina Casper and Close, {Graeme L.} and Colbert, {Lisa H.} and Cooper, {Jamie A.} and Richard Cooper and Prasangi Dabare and Das, {Sai Krupa} and Davies, {Peter S. W.} and Sanjoy Deb and Nystr{\"o}m, {Christine Delisle} and William Dietz and Dugas, {Lara R.} and Simon Eaton and Ulf Ekelund and Hamdouchi, {Asmaa El} and Sonja Entringer and Terrence Forrester and Fudge, {Barry W.} and Melanie Gillingham and Goris, {Annelies H.} and Michael Gurven and Hinke Haisma and Catherine Hambly and Hoffman, {Daniel J.} and Hoos, {Marije B.} and Sumei Hu and Noorjehan Joonas and Annemiek Joosen and Peter Katzmarzyk and Kempen, {Kitty P.} and Misaka Kimura and Kraus, {William E.} and Wantanee Kriengsinyos and Rebecca Kuriyan and Kushner, {Robert F.} and Lambert, {Estelle V.} and Pulani Lanerolle and Larsson, {Christel L.} and Nader Lessan and Marie L{\"o}f and Martin, {Corby K.} and Eric Matsiko and Meijer, {Gerwin A.} and Morehen, {James C.} and Morton, {James P.} and Aviva Must and Marian Neuhouser and Nicklas, {Theresa A.} and Ojiambo, {Robert M.} and Pietilainen, {Kirsi H.} and Pitsiladis, {Yannis P.} and Jacob Plange-Rhule and Guy Plasqui and Prentice, {Ross L.} and Roberto Rabinovich and Racette, {Susan B.} and Raichen, {David A.} and Eric Ravussin and Leanne Redman and Reilly, {John J.} and Reynolds, {Rebecca M.} and Susan Roberts and Dulani Samaranayake and Sardinha, {Lu{\'i}s B.} and Schuit, {Albertine J.} and Silva, {Analiza M.} and Srishti Sinha and Sj{\"o}din, {Anders M.} and Eric Stice and Albert Stunkard and Urlacher, {Samuel S.} and Valencia, {Mauro Eduardo} and Giulio Valenti and {van Etten}, {Ludo M.} and {Van Mil}, {Edgar A.} and Verbunt, {Jeanine A.} and Wells, {Jonathan C. K.} and George Wilson and Brian Wood and Tsukasa Yoshida and Xueying Zhang and Alexia Murphy-Alford and Cornelia Loechl and Amy Luke and Herman Pontzer and Jennifer Rood and Hiroyuki Sagayama and Westerterp, {Klaas R.} and Wong, {William W.} and Yosuke Yamada and Speakman, {John R.} and {IAEA DLW Database Consortium}",

note = "Funding information: The authors also gratefully acknowledge funding from the Chinese Academy of Sciences (grant no. CAS153E11KYSB20190045) to J.R.S. and the US National Science Foundation (grant no. BCS-1824466) awarded to H.P. Publisher Copyright: {\textcopyright} 2023 The Authors.",

year = "2023",

month = sep,

day = "20",

doi = "10.1098/rsbl.2023.0152",

language = "English",

volume = "19",

journal = "Biology Letters",

issn = "1744-9561",

publisher = "The Royal Society",

number = "9",

}

Halsey, LG, Careau, V, Ainslie, PN, Alemán-Mateo, H, Andersen, LF, Anderson, LJ, Arab, L, Baddou, I, Bandini, L, Bedu-Addo, K, Blaak, EE, Blanc, S, Bonomi, AG, Bouten, CVC, Bovet, P, Brage, S, Buchowski, MS, Butte, NF, Camps, SG, Casper, R, Close, GL, Colbert, LH, Cooper, JA, Cooper, R, Dabare, P, Das, SK, Davies, PSW, Deb, S, Nyström, CD, Dietz, W, Dugas, LR, Eaton, S, Ekelund, U, Hamdouchi, AE, Entringer, S, Forrester, T, Fudge, BW, Gillingham, M, Goris, AH, Gurven, M, Haisma, H, Hambly, C, Hoffman, DJ, Hoos, MB, Hu, S, Joonas, N, Joosen, A, Katzmarzyk, P, Kempen, KP, Kimura, M, Kraus, WE, Kriengsinyos, W, Kuriyan, R, Kushner, RF, Lambert, EV, Lanerolle, P, Larsson, CL, Lessan, N, Löf, M, Martin, CK, Matsiko, E, Meijer, GA, Morehen, JC, Morton, JP, Must, A, Neuhouser, M, Nicklas, TA, Ojiambo, RM, Pietilainen, KH, Pitsiladis, YP, Plange-Rhule, J, Plasqui, G, Prentice, RL, Rabinovich, R, Racette, SB, Raichen, DA, Ravussin, E, Redman, L, Reilly, JJ, Reynolds, RM, Roberts, S, Samaranayake, D, Sardinha, LB, Schuit, AJ, Silva, AM, Sinha, S, Sjödin, AM, Stice, E, Stunkard, A, Urlacher, SS, Valencia, ME, Valenti, G, van Etten, LM, Van Mil, EA, Verbunt, JA, Wells, JCK, Wilson, G, Wood, B, Yoshida, T, Zhang, X, Murphy-Alford, A, Loechl, C, Luke, A, Pontzer, H, Rood, J, Sagayama, H, Westerterp, KR, Wong, WW, Yamada, Y, Speakman, JR & IAEA DLW Database Consortium 2023, 'Greater male variability in daily energy expenditure develops through puberty', Biology Letters, vol. 19, no. 9, 20230152. https://doi.org/10.1098/rsbl.2023.0152

TY - JOUR

T1 - Greater male variability in daily energy expenditure develops through puberty

AU - Halsey, Lewis G.

AU - Careau, Vincent

AU - Ainslie, Philip N.

AU - Alemán-Mateo, Heliodoro

AU - Andersen, Lene F.

AU - Anderson, Liam J.

AU - Arab, Leonore

AU - Baddou, Issad

AU - Bandini, Linda

AU - Bedu-Addo, Kweku

AU - Blaak, Ellen E.

AU - Blanc, Stephane

AU - Bonomi, Alberto G.

AU - Bouten, Carlijn V. C.

AU - Bovet, Pascal

AU - Brage, Soren

AU - Buchowski, Maciej S.

AU - Butte, Nancy F.

AU - Camps, Stephan G.

AU - Casper, Regina

AU - Close, Graeme L.

AU - Colbert, Lisa H.

AU - Cooper, Jamie A.

AU - Cooper, Richard

AU - Dabare, Prasangi

AU - Das, Sai Krupa

AU - Davies, Peter S. W.

AU - Deb, Sanjoy

AU - Nyström, Christine Delisle

AU - Dietz, William

AU - Dugas, Lara R.

AU - Eaton, Simon

AU - Ekelund, Ulf

AU - Hamdouchi, Asmaa El

AU - Entringer, Sonja

AU - Forrester, Terrence

AU - Fudge, Barry W.

AU - Gillingham, Melanie

AU - Goris, Annelies H.

AU - Gurven, Michael

AU - Haisma, Hinke

AU - Hambly, Catherine

AU - Hoffman, Daniel J.

AU - Hoos, Marije B.

AU - Hu, Sumei

AU - Joonas, Noorjehan

AU - Joosen, Annemiek

AU - Katzmarzyk, Peter

AU - Kempen, Kitty P.

AU - Kimura, Misaka

AU - Kraus, William E.

AU - Kriengsinyos, Wantanee

AU - Kuriyan, Rebecca

AU - Kushner, Robert F.

AU - Lambert, Estelle V.

AU - Lanerolle, Pulani

AU - Larsson, Christel L.

AU - Lessan, Nader

AU - Löf, Marie

AU - Martin, Corby K.

AU - Matsiko, Eric

AU - Meijer, Gerwin A.

AU - Morehen, James C.

AU - Morton, James P.

AU - Must, Aviva

AU - Neuhouser, Marian

AU - Nicklas, Theresa A.

AU - Ojiambo, Robert M.

AU - Pietilainen, Kirsi H.

AU - Pitsiladis, Yannis P.

AU - Plange-Rhule, Jacob

AU - Plasqui, Guy

AU - Prentice, Ross L.

AU - Rabinovich, Roberto

AU - Racette, Susan B.

AU - Raichen, David A.

AU - Ravussin, Eric

AU - Redman, Leanne

AU - Reilly, John J.

AU - Reynolds, Rebecca M.

AU - Roberts, Susan

AU - Samaranayake, Dulani

AU - Sardinha, Luís B.

AU - Schuit, Albertine J.

AU - Silva, Analiza M.

AU - Sinha, Srishti

AU - Sjödin, Anders M.

AU - Stice, Eric

AU - Stunkard, Albert

AU - Urlacher, Samuel S.

AU - Valencia, Mauro Eduardo

AU - Valenti, Giulio

AU - van Etten, Ludo M.

AU - Van Mil, Edgar A.

AU - Verbunt, Jeanine A.

AU - Wells, Jonathan C. K.

AU - Wilson, George

AU - Wood, Brian

AU - Yoshida, Tsukasa

AU - Zhang, Xueying

AU - Murphy-Alford, Alexia

AU - Loechl, Cornelia

AU - Luke, Amy

AU - Pontzer, Herman

AU - Rood, Jennifer

AU - Sagayama, Hiroyuki

AU - Westerterp, Klaas R.

AU - Wong, William W.

AU - Yamada, Yosuke

AU - Speakman, John R.

AU - IAEA DLW Database Consortium

N1 - Funding information: The authors also gratefully acknowledge funding from the Chinese Academy of Sciences (grant no. CAS153E11KYSB20190045) to J.R.S. and the US National Science Foundation (grant no. BCS-1824466) awarded to H.P. Publisher Copyright: © 2023 The Authors.

PY - 2023/9/20

Y1 - 2023/9/20

N2 - There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decrease in the degree of GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

AB - There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decrease in the degree of GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

KW - age

KW - height

KW - inter-individual variation

KW - morphometry

KW - weight

UR - http://www.scopus.com/inward/record.url?scp=85171901906&partnerID=8YFLogxK

U2 - 10.1098/rsbl.2023.0152

DO - 10.1098/rsbl.2023.0152

M3 - Journal article

C2 - 37727077

AN - SCOPUS:85171901906

SN - 1744-9561

VL - 19

JO - Biology Letters

JF - Biology Letters

IS - 9

M1 - 20230152

ER -

Greater male variability in daily energy expenditure develops through puberty

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UN SDGs

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