Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis

Tarka M, Günther A, Niemelae PT, Nakagawa S, Noble DWA (2018)

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Tarka, Maja; Günther, AnjaUniBi; Niemelae, Petri T.; Nakagawa, Shinichi; Noble, Daniel W. A.
Abstract / Bemerkung
The pace-of-life syndrome (POLS) hypothesis predicts that behavior and physiology covary with life history. Evidence for such covariation is contradictory, possibly because systematic sources of variation (e.g. sex) have been neglected. Sexes often experience different selection pressures leading to sex-specific allocation between reproduction and self-maintenance, facilitating divergence in life-history. Sex-specific differences in means and possibly variances may therefore play a key role in the POLS framework. We investigate whether sexes differ in means and variances along the fast-slow pace-of-life continuum for life history and physiological and behavioral traits. In addition, we test whether social and environmental characteristics such as breeding strategy, mating system, and study environment explain heterogeneity between the sexes. Using meta-analytic methods, we found that populations with a polygynous mating system or for studies conducted on wild populations, males had a faster pace-of-life for developmental life-history traits (e.g., growth rate), behavior, and physiology. In contrast, adult life-history traits (e.g., lifespan) were shifted towards faster pace-of-life in females, deviating from the other trait categories. Phenotypic variances were similar between the sexes across trait categories and were not affected by mating system or study environment. Breeding strategy did not influence sex differences in variances or means. We discuss our results in the light of sex-specific selection that might drive sex-specific differences in pace-of-life and ultimately POLS.
Life history; Pace-of-life syndrome; Pace-of-life; Phenotypic variation; Sexual selection; Sexual dimorphism
UNSP 132
Page URI


Tarka M, Günther A, Niemelae PT, Nakagawa S, Noble DWA. Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY. 2018;72(8): UNSP 132.
Tarka, M., Günther, A., Niemelae, P. T., Nakagawa, S., & Noble, D. W. A. (2018). Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 72(8), UNSP 132. doi:10.1007/s00265-018-2534-2
Tarka, Maja, Günther, Anja, Niemelae, Petri T., Nakagawa, Shinichi, and Noble, Daniel W. A. 2018. “Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis”. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 72 (8): UNSP 132.
Tarka, M., Günther, A., Niemelae, P. T., Nakagawa, S., and Noble, D. W. A. (2018). Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 72:UNSP 132.
Tarka, M., et al., 2018. Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 72(8): UNSP 132.
M. Tarka, et al., “Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis”, BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, vol. 72, 2018, : UNSP 132.
Tarka, M., Günther, A., Niemelae, P.T., Nakagawa, S., Noble, D.W.A.: Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY. 72, : UNSP 132 (2018).
Tarka, Maja, Günther, Anja, Niemelae, Petri T., Nakagawa, Shinichi, and Noble, Daniel W. A. “Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis”. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 72.8 (2018): UNSP 132.

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Population-, sex- and individual level divergence in life-history and activity patterns in an annual killifish.
Thoré ESJ, Grégoir AF, Adriaenssens B, Philippe C, Stoks R, Brendonck L, Pinceel T., PeerJ 7(), 2019
PMID: 31293828

111 References

Daten bereitgestellt von Europe PubMed Central.

Sexual conflict, life span, and aging
Adler M, Bonduriansky R., 2014

Andersson M., 1994

Arnqvist G, Rowe L., 2005
Intra-sexual selection in Drosophila.
BATEMAN AJ., Heredity (Edinb) 2(Pt. 3), 1948
PMID: 18103134
Are animal personality traits linked to life-history productivity?
Biro PA, Stamps JA., Trends Ecol. Evol. (Amst.) 23(7), 2008
PMID: 18501468
Evidence for a `fast-slow’continuum of life-history traits among parasitoid hymenoptera
Blackburn T., 1991

Blaxter K., 1989
Sexual selection, sexual conflict and the evolution of ageing and life span
Bonduriansky R, Maklakov A, Zajitschek F, Brooks R., 2008
The evolution of semelparity
Bonnet X., 2011
Life history evolution, reproduction, and the origins of sex-dependent aging and longevity.
Brooks RC, Garratt MG., Ann. N. Y. Acad. Sci. 1389(1), 2016
PMID: 28009055
Environmental quality and evolutionary potential: lessons from wild populations
Charmantier A, Garant D., 2005

Clutton-Brock T., 2016
Sex differences in ageing in natural populations of vertebrates
Clutton-Brock T, Isvaran K., 2007
Sexual selection and the potential reproductive rates of males and females.
Clutton-Brock TH, Vincent AC., Nature 351(6321), 1991
PMID: 2027382
The behavioural ecology of personality: consistent individual differences from an adaptive perspective
Dall SRX, Houston AL, McNamara JM., 2004
Are personality differences in a small iteroparous mammal maintained by a life-history trade-off?
Dammhahn M., 2012
Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life-history
Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D., 2018
Ecological Character Displacement between the Sexes.
De Lisle SP, Rowe L., Am. Nat. 186(6), 2015
PMID: 26655977

Bias in meta-analysis detected by a simple, graphical test.
Egger M, Davey Smith G, Schneider M, Minder C., BMJ 315(7109), 1997
PMID: 9310563

Fairbairn D, Blanckenhorn W, Székely T., 2007
Sperm competition drives the evolution of suicidal reproduction in mammals
Fisher D, Dickman C, Jones M, Blomberg S., 2013
Selection in captive populations
Frankham R, Hemmer H, Ryder OA, Cothran EG, Soulé ME, Murray ND, Snyder M., 1986
Mother's curse: the effect of mtDNA on individual fitness and population viability.
Gemmell NJ, Metcalf VJ, Allendorf FW., Trends Ecol. Evol. (Amst.) 19(5), 2004
PMID: 16701262
Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments
Ghalambor CK, McKay JK, Carroll SP, Reznick DN., 2007
The phylogenetic regression.
Grafen A., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 326(1233), 1989
PMID: 2575770
Mating systems, philopatry and dispersal in birds and mammals
Greenwood P., 1980
Regularization Paths for Generalized Linear Models via Coordinate Descent.
Friedman J, Hastie T, Tibshirani R., J Stat Softw 33(1), 2010
PMID: 20808728
Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate.
Hamalainen A, Dammhahn M, Aujard F, Eberle M, Hardy I, Kappeler PM, Perret M, Schliehe-Diecks S, Kraus C., Proc. Biol. Sci. 281(1791), 2014
PMID: 25100693
Evolution of sex-specific pace-of-life syndromes: causes and consequences
Hämäläinen A, Immonen E, Tarka M, Schuett W., 2018
The meta-analysis of response ratios in experimental ecology
Hedges LV, Gurevitch J, Curtis PS., 1999
The evolution of sexual dimorphism in animals: Hypotheses and tests.
Hedrick AV, Temeles EJ., Trends Ecol. Evol. (Amst.) 4(5), 1989
PMID: 21227335
Quantifying heterogeneity in a meta-analysis
Higgins JPT, Thompson SG., 2002

Synthesis of phylogeny and taxonomy into a comprehensive tree of life
Hinchcliff CE, Smith SA, Allman JF., 2015
Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms.
Immonen E, Hamalainen A, Schuett W, Tarka M., Behav. Ecol. Sociobiol. (Print) 72(3), 2018
PMID: 29576676
Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution.
Innocenti P, Morrow EH, Dowling DK., Science 332(6031), 2011
PMID: 21566193
Personality and innate immune defenses in a wild bird: evidence for the pace-of-life hypothesis
Jacques-Hamilton R, Hall M, Buttemer W, Matson KD, Gonçalves A, Mulder RA, Peters A., 2017
Covariances between relatives due to sex-linked genes.
James JW., Biometrics 29(3), 1973
PMID: 4806359
Darwinian sex roles confirmed across the animal kingdom.
Janicke T, Haderer IK, Lajeunesse MJ, Anthes N., Sci Adv 2(2), 2016
PMID: 26933680
Physiological underpinnings associated with differences in pace of life and metabolic rate in north temperate and neotropical birds.
Jimenez AG, Cooper-Mullin C, Calhoon EA, Williams JB., J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 184(5), 2014
PMID: 24671698
Unsociable juvenile male three-spined sticklebacks grow more attractive
Kim S-Y, Velando A., 2016
Parental investment, sexual selection and sex ratios
Kokko H, Jennions M., 2008
Eunuchs are better fighters
Kralj-Fišer S, Gregoric M, Zhang S, Li D, Kuntner M., 2011
Why anisogamy drives ancestral sex roles.
Lehtonen J, Parker GA, Scharer L., Evolution 70(5), 2016
PMID: 27110661

Maynard J., 1982
Intra-individual variability in fecal cortisol metabolites varies with lifetime exploration and reproductive life history in eastern chipmunks (Tamias striatus)
Montiglio P-O, Garant D, Pelletier F, Réale D., 2014


Field metabolic rate and food requirement scaling in mammals and birds
Nagy K., 1987
Methodological issues and advances in biological meta-analysis
Nakagawa S, Santos ESA., 2012
Coefficient of determination R and intra-class correlation coefficient ICC from generalized linear mixed-effects models revisited and expanded
Nakagawa S, Schielzeth H., 2016
Meta-analysis of variation: ecological and evolutionary applications and beyond
Nakagawa S, Poulin R, Mengersen K, Reinhold K, Engqvist L, Lagisz M, Senior AM., 2015
Meta-evaluation of meta-analysis: ten appraisal questions for biologists.
Nakagawa S, Noble DW, Senior AM, Lagisz M., BMC Biol. 15(1), 2017
PMID: 28257642

Nelson RJ., 2011
Artificial environments and the study of 'adaptive' personalities.
Niemela PT, Dingemanse NJ., Trends Ecol. Evol. (Amst.) 29(5), 2014
PMID: 24629720
Meta-analysis reveals weak associations between intrinsic state and personality.
Niemela PT, Dingemanse NJ., Proc. Biol. Sci. 285(1873), 2018
PMID: 29491175
Personality pace-of-life hypothesis: testing genetic associations among personality and life history
Niemelä PT, Dingemanse NJ, Alioravainen N, Vainikka A, Kortet R., 2013
Nonindependence and sensitivity analyses in ecological and evolutionary meta-analyses.
Noble DWA, Lagisz M, O'dea RE, Nakagawa S., Mol. Ecol. 26(9), 2017
PMID: 28133832
The role of non-genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps.
O'Dea RE, Noble DWA, Johnson SL, Hesselson D, Nakagawa S., Environ Epigenet 2(1), 2016
PMID: 29492283
Effect size in ecological experiments: the application of biological models in meta-analysis.
Osenberg CW, Sarnelle O, Cooper SD., Am. Nat. 150(6), 1997
PMID: 18811337
Ancient ecological diversification explains life-history variation among living birds
Owens I, Bennett P., 1995
Sexual selection and sexual conflict
Parker G., 1979
Value of captive populations for quantitative genetics research.
Pelletier F, Reale D, Watters J, Boakes EH, Garant D., Trends Ecol. Evol. (Amst.) 24(5), 2009
PMID: 19269058
Costs of sexual selection in natural populations of mammals
Promislow D., 1992
Mate choice, sexual conflict, and evolution of senescence.
Promislow D., Behav. Genet. 33(2), 2003
PMID: 14574152
Living fast and dying young: a comparative analysis of life-history variation among mammals
Promislow D, Harvey P., 1990
Sex and environmental sensitivity in blue tit nestlings.
Raberg L, Stjernman M, Nilsson JA., Oecologia 145(3), 2005
PMID: 15965752
Integrating animal temperament within ecology and evolution.
Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ., Biol Rev Camb Philos Soc 82(2), 2007
PMID: 17437562
Personality and the emergence of the pace-of-life syndrome concept at the population level.
Reale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365(1560), 2010
PMID: 21078657
The variability is in the sex chromosomes.
Reinhold K, Engqvist L., Evolution 67(12), 2013
PMID: 24299417
The evolution of sex-specific immune defences
Restif O, Amos W., 2010

The physiology/life-history nexus
Ricklefs R, Wikelski M., 2002

Roff D., 2002
Is basal metabolic rate associated with recruit production and survival in free-living house sparrows?
Rønning B, Broggi J, Bech C, Moe B, Ringsby TH, Pärn H, Hagen IJ, Sæther BE, Jensen H., 2016
The lek paradox and the capture of genetic variance by condition dependent traits
Rowe L, Houle D., 1996
Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis
Royauté R, Berdal MA, Garrison CR, Dochtermann NA., 2018
Energetic trade-offs and feedbacks between behavior and metabolism influence correlations between pace-of-life attributes
Salzman TC, McLaughlin AL, Westneat DF, Crowley PH., 2018
Hidden reaction norms, cryptic genetic variation, and evolvability.
Schlichting CD., Ann. N. Y. Acad. Sci. 1133(), 2008
PMID: 18559822
Sexual selection and animal personality.
Schuett W, Tregenza T, Dall SR., Biol Rev Camb Philos Soc 85(2), 2009
PMID: 19922534
An Overlooked Consequence of Dietary Mixing: A Varied Diet Reduces Interindividual Variance in Fitness.
Senior AM, Nakagawa S, Lihoreau M, Simpson SJ, Raubenheimer D., Am. Nat. 186(5), 2015
PMID: 26655777
Behavioral syndromes: an ecological and evolutionary overview.
Sih A, Bell A, Johnson JC., Trends Ecol. Evol. (Amst.) 19(7), 2004
PMID: 16701288
Fitness consequences of personality: a meta-analysis
Smith BR, Blumstein DT., 2008
The physiological costs of reproduction in small mammals.
Speakman JR., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363(1490), 2008
PMID: 17686735
The influence of size and phylogeny on patterns of covariation among life-history traits in the mammals
Stearns S., 1983

Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone house wrens
Tieleman B, Dijkstra T, Lasky J, Mauck RA, Visser GH, Williams JB., 2006
The genetics of gender and life span.
Tower J, Arbeitman M., J. Biol. 8(4), 2009
PMID: 19439039

Conducting meta-analyses in R with the metafor package
Viechtbauer W., 2010
Tropical birds have a slow pace of life
Wiersma P, Muñoz-Garcia A, Walker A, Williams J., 2007
Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes
Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E., 2003
Functional linkages for the pace of life, life-history, and environment in birds.
Williams JB, Miller RA, Harper JM, Wiersma P., Integr. Comp. Biol. 50(5), 2010
PMID: 21558245
The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies
Wingfield J, Hegner R, Dufty AJ, Ball G., 1990
Linking lab activity with growth and movement in the wild: explaining pace-of-life in a trout stream
Závorka L, Aldvén D, Näslund J, Höjesjö J, Johsson JI., 2015

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 30100667
PubMed | Europe PMC

Suchen in

Google Scholar