Reproductive fitness is associated with female chronotype in a songbird

Research on biological rhythms has revealed widespread variation in diel timing within populations. Repeatable individual chronotypes have been linked to performance in humans but, in free-living species, benefits of chronotype are poorly understood. To address this gap, we investigated fitness correlates of incubation patterns in female songbirds (great tit, Parus major) at urban and forest sites. We confirm repeatable chronotypes (r ≥ 0.31) and show novel links between chronotype and reproductive success. In both habitats, females that started activity earlier in the day raised more fledglings. We also observed that forest females started their day at a similar time throughout the breeding season, whereas urban females tied their onset of activity closely to sunrise. Our study points to possible mechanisms that underlie chronotype variation and provides sought-after evidence for its relevance to fitness.

[1]  M. Eens,et al.  No relationship between chronotype and timing of breeding when variation in daily activity patterns across the breeding season is taken into account , 2022, Ecology and evolution.

[2]  J. Sanz,et al.  Impacts of ambient temperature and clutch size on incubation behaviour onset in a female‐only incubator songbird , 2021 .

[3]  C. Cooper,et al.  Deconstructing incubation behaviour in response to ambient temperature over different timescales , 2021, Journal of Avian Biology.

[4]  Luke L. Powell,et al.  Bitter fruits of hard labour: diet metabarcoding and telemetry reveal that urban songbirds travel further for lower-quality food , 2020, Oecologia.

[5]  C. Cooper,et al.  Night conditions affect morning incubation behaviour differently across a latitudinal gradient , 2020 .

[6]  C. Maury,et al.  Plasticity in diurnal activity and temporal phenotype during parental care in European starlings, Sturnus vulgaris , 2020, Animal Behaviour.

[7]  Eva C. Winnebeck,et al.  Chronotype and Social Jetlag: A (Self-) Critical Review , 2019, Biology.

[8]  Samuel E. Jones,et al.  Genome-wide association analyses of chronotype in 697,828 individuals provides insights into circadian rhythms , 2019, Nature Communications.

[9]  J. Meijer,et al.  Biological clock function is linked to proactive and reactive personality types , 2018, BMC Biology.

[10]  Justin S. Brashares,et al.  The influence of human disturbance on wildlife nocturnality , 2018, Science.

[11]  C. Cooper,et al.  ‘Green incubation': avian offspring benefit from aromatic nest herbs through improved parental incubation behaviour , 2018, Proceedings of the Royal Society B: Biological Sciences.

[12]  J. Alós,et al.  Fitness consequences of fish circadian behavioural variation in exploited marine environments , 2018, PeerJ.

[13]  P. Capilla-Lasheras.  incR: a new R package to analyse incubation behaviour , 2018, bioRxiv.

[14]  M. Visser,et al.  Two sides of a coin: ecological and chronobiological perspectives of timing in the wild , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  D. Hazlerigg,et al.  Timing as a sexually selected trait: the right mate at the right moment , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  Martin A. Stoffel,et al.  rptR: repeatability estimation and variance decomposition by generalized linear mixed‐effects models , 2017 .

[17]  B. Kempenaers,et al.  Singing from North to South: Latitudinal variation in timing of dawn singing under natural and artificial light conditions , 2017, The Journal of animal ecology.

[18]  M. Hau,et al.  Early to rise, early to breed: a role for daily rhythms in seasonal reproduction , 2017 .

[19]  C. Pollock,et al.  Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus) , 2017, Scientific Reports.

[20]  C. Pollock,et al.  Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits , 2017, Front. Ecol. Evol..

[21]  Vinod Kumar,et al.  Neural control of daily and seasonal timing of songbird migration , 2017, Journal of Comparative Physiology A.

[22]  Vinod Kumar,et al.  Neural control of daily and seasonal timing of songbird migration , 2017, Journal of Comparative Physiology A.

[23]  J. Vitale,et al.  Chronotype, Physical Activity, and Sport Performance: A Systematic Review , 2017, Sports Medicine.

[24]  Andrea Campos-Candela,et al.  Repeatability of circadian behavioural variation revealed in free-ranging marine fish , 2017, Royal Society Open Science.

[25]  J. Senar,et al.  More Ornamented Great Tit Parus major Fathers Start Feeding Their Offspring Earlier , 2016, Ardea.

[26]  N. P. Huffeldt,et al.  Sex-specific, inverted rhythms of breeding-site attendance in an Arctic seabird , 2016, Biology Letters.

[27]  K. Oers,et al.  Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird , 2015 .

[28]  B. Kempenaers,et al.  Sources of intraspecific variation in sleep behaviour of wild great tits , 2015, Animal Behaviour.

[29]  E. Facer-Childs,et al.  The Impact of Circadian Phenotype and Time since Awakening on Diurnal Performance in Athletes , 2015, Current Biology.

[30]  K. Gaston,et al.  Biogeography of time partitioning in mammals , 2014, Proceedings of the National Academy of Sciences.

[31]  Jelmer M. Samplonius,et al.  Artificial night lighting rather than traffic noise affects the daily timing of dawn and dusk singing in common European songbirds , 2014 .

[32]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[33]  Bart Kranstauber,et al.  Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds. , 2014, The Journal of animal ecology.

[34]  W. Cresswell,et al.  Latitudinal variation in day length and working day length has a confounding effect when comparing nest attentiveness in tropical and temperate species , 2014, Journal of Ornithology.

[35]  H. Dowse,et al.  Clocks for the city: circadian differences between forest and city songbirds , 2013, Proceedings of the Royal Society B: Biological Sciences.

[36]  C. Cooper,et al.  Avian Incubation Patterns Reflect Temporal Changes in Developing Clutches , 2013, PloS one.

[37]  M. Visser,et al.  Effects of Temperature on Circadian Clock and Chronotype: An Experimental Study on a Passerine Bird , 2012, Chronobiology international.

[38]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[39]  M. Visser,et al.  Heritable circadian period length in a wild bird population , 2010, Proceedings of the Royal Society B: Biological Sciences.

[40]  B. Kempenaers,et al.  Artificial Night Lighting Affects Dawn Song, Extra-Pair Siring Success, and Lay Date in Songbirds , 2010, Current Biology.

[41]  M. T. Murphy,et al.  Dawn song of the eastern kingbird: an honest signal of male quality? , 2008, Animal Behaviour.

[42]  Steven A. Brown,et al.  Molecular insights into human daily behavior , 2008, Proceedings of the National Academy of Sciences.

[43]  Till Roenneberg,et al.  The human circadian clock entrains to sun time , 2007, Current Biology.

[44]  Mark W. Miller.  Apparent Effects of Light Pollution on Singing Behavior of American Robins , 2006 .

[45]  T. Dayan,et al.  Partitioning of Time as an Ecological Resource , 2003 .

[46]  A. Wirz-Justice,et al.  Life between Clocks: Daily Temporal Patterns of Human Chronotypes , 2003, Journal of biological rhythms.

[47]  S. L. Lima,et al.  Foraging routines of small birds in winter: a theoretical investigation , 1994 .

[48]  A. Gosler.  The Great Tit , 1993 .

[49]  R. Mace.  Importance of female behaviour in the dawn chorus , 1986, Animal Behaviour.

[50]  A. Kacelnik.  The foraging efficiency of great tits (Parus major L.) in relation to light intensity , 1979, Animal Behaviour.

[51]  S. Daan,et al.  University of Groningen Circadian Rhythms of Locomotor Activity in Captive Birds and Mammals , 2004 .

[52]  H Meiners,et al.  [Effects of temperature]. , 1973, ZWR.

[53]  M. Menaker,et al.  Entrainment of Circadian Rhythms by Sound in Passer domesticus , 1966, Science.

[54]  B. Helm.  Clocks and Calendars in Birds , 2020 .

[55]  D. Arnaud,et al.  Latitudinal variation in timing of dawn singing under natural and artificial light conditions , 2017 .

[56]  V. Cassone.  Avian Circadian Organization , 2015 .

[57]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[58]  E. Gwinner.  Periodicity of a circadian rhythm in birds by species-specific song cycles (Aves, Fringillidae: Carduelis spinus, Serinus serinus) , 2005, Experientia.

[59]  A. Houston,et al.  Optimal daily routines of singing and foraging in a bird singing to attract a mate , 2004, Behavioral Ecology and Sociobiology.

[60]  C. Ehret,et al.  Circadian cybernetics. III. Circadian cybernetic studies of the mammalian clock. B. The sense of time: evidence for its molecular basis in the eukaryotic gene action system , 1972 .