Abstract
Parental investment theory predicts that observed levels of parental care afforded to offspring are set by the benefits (to offspring quality and survival) relative to the costs (to parental survival or future reproduction). Although difficult to document in mammals, there is often substantial individual variation in the amount of parental care within species. We measured the impact of individual variation in maternal care (“attentiveness” towards offspring or maternal motivation) on offspring growth and survival in a wild population of North American red squirrels (Tamiasciurus hudsonicus). We used latency to return to pups following a nest intrusion as a measure of maternal attentiveness to pups. We found this behavior to be repeatable within individuals suggesting this behavior is a personality trait or a “maternal style.” In this population, postnatal growth rate is important for pup overwinter survival. Pups from large litters grew faster if they had a highly attentive mother, indicating that maternal care can mitigate the trade-off between litter size and offspring growth and potentially improve survival of pups. Additionally, more attentive mothers had slightly higher lifetime reproductive success than less attentive mothers. These results highlight important fitness effects of having a highly attentive mother and show that maternal care can alter a fundamental life history trade-off between offspring quantity and quality.
Significance statement
It pays to be attentive to your pups as a squirrel mom. In a long-term study of a wild population of North American red squirrels, we tested whether maternal behavior was predictive of growth rate and survival of offspring. To do this, we observed maternal attentiveness towards offspring by recording the time until the mother returned to her pups following a nest intrusion by researchers. We found repeatable individual variation in maternal attentiveness suggesting consistent “maternal styles” among individuals. Mothers who returned faster to pups following a nest intrusion produced faster growing pups and were able to produce larger fast-growing litters. Over their entire lifetime, attentive mothers also had more offspring survive to adulthood.
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Data availability
The datasets generated for the current study are available in a figshare repository after April 13, 2022: https://doi.org/10.6084/m9.figshare.12118704. The datasets analyzed during the current study are available earlier than this date from the corresponding author on reasonable request.
References
Bales K, French JA, Dietz JM (2002) Explaining variation in maternal care in a cooperatively breeding mammal. Anim Behav 63:453–461. https://doi.org/10.1006/anbe.2001.1954
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. https://doi.org/10.1016/j.anbehav.2008.12.022
Bergeron P, Baeta R, Pelletier F, Réale D, Garant D (2011) Individual quality: tautology or biological reality? J Anim Ecol 80:361–364. https://doi.org/10.1111/j.1365-2656.2010.01770.x
Berteaux D, Boutin S (2000) Breeding dispersal in female North American red squirrels. Ecology 81:1311–1326. https://doi.org/10.1890/0012-9658(2000)081[1311:BDIFNA]2.0.CO;2
Boutin S, Larsen KW (1993) Does food availability affect growth and survival of males and females differently in a promiscuous small mammal, Tamiasciurus hudsonicus? J Anim Ecol 62:364–370. https://doi.org/10.2307/5367
Boutin S, Larsen KW, Berteaux D (2000) Anticipatory parental care: acquiring resources for offspring prior to conception. Proc R Soc Lond B 267:2081–2085. https://doi.org/10.1098/rspb.2000.1252
Boutin S, Wauters LA, McAdam AG, Humphries MM, Tosi G, Dhondt AA (2006) Anticipatory reproduction and population growth in seed predators. Science 314:1928–1930. https://doi.org/10.1126/science.1135520
Champagne FA, Curley JP, Keverne EB, Bateson PPG (2007) Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav 91:325–334. https://doi.org/10.1016/j.physbeh.2007.03.014
Charnov EL, Ernest SKM (2006) The offspring-size/clutch-size trade-off in mammals. Am Nat 167:578–582. https://doi.org/10.1086/501141
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Cooper EB, Taylor RW, Kelley AD, Martinig AR, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2017) Personality is correlated with natal dispersal in North American red squirrels (Tamiasciurus hudsonicus). Behaviour 154:939–961. https://doi.org/10.1163/1568539X-00003450
Dantzer B, Boutin S, Humphries MM, McAdam AG (2012) Behavioral responses of territorial red squirrels to natural and experimental variation in population density. Behav Ecol Sociobiol 66:865–878. https://doi.org/10.1007/s00265-012-1335-2
Dantzer B, Newman AEM, Boonstra R, Palme R, Boutin S, Humphries MM, McAdam AG (2013) Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340:1215–1217. https://doi.org/10.1126/science.1235765
Datta S (2005) Estimating the mean life time using right censored data. Stat Methodol 2:65–69. https://doi.org/10.1016/j.stamet.2004.11.003
David M, Pinxten R, Martens T, Eens M (2015) Exploration behavior and parental effort in wild great tits: partners matter. Behav Ecol Sociobiol 69:1085–1095. https://doi.org/10.1007/s00265-015-1921-1
Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252. https://doi.org/10.5253/arde.v68.p225
Fairbanks LA, Ackles PK (2012) What is a good mother? Adaptive variation in maternal behavior of primates. Psychol Sci 2:179–183
Fisher DN, Boutin S, Dantzer B, Humphries MM, Lane JE, McAdam AG (2017) Multilevel and sex-specific selection on competitive traits in North American red squirrels. Evolution 71:1841–1854. https://doi.org/10.1111/evo.13270
Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM (2010) The functional response of a hoarding seed predator to mast seeding. Ecology 91:2673–2683. https://doi.org/10.1890/09-1816.1
Fletcher QE, Landry-Cuerrier M, Boutin S, McAdam AG, Speakman JR, Humphries MM (2013) Reproductive timing and reliance on hoarded capital resources by lactating red squirrels. Oecologia 173:1203–1215. https://doi.org/10.1007/s00442-013-2699-3
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks
Grafen A (1988) On the use of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. Studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 454–471
Guillemette CU, Fletcher QE, Boutin S, Hodges RM, McAdam AG, Humphries MM (2009) Lactating red squirrels experiencing high heat load occupy less insulated nests. Biol Lett 5:166–168. https://doi.org/10.1098/rsbl.2008.0592
Hadfield JD (2008) Estimating evolutionary parameters when viability selection is operating. Proc R Soc Lond B 275:723–734. https://doi.org/10.1098/rspb.2007.1013
Hard E, Hansen S (1985) Reduced fearfulness in the lactating rat. Physiol Behav 35:641–643. https://doi.org/10.1016/0031-9384(85)90155-6
Hendrix JG, Fisher DN, Martinig AR, Boutin S, Dantzer LJE, McAdam AG (2020) Territory acquisition mediates the influence of predators and climate on juvenile red squirrel survival. J Anim Ecol. https://doi.org/10.1111/1365-2656.13209
Humphries MM, Boutin S (1996) Reproductive demands and mass gains: a paradox in female red squirrels (Tamiasciurus hudsonicus). J Anim Ecol 65:332–338
Humphries MM, Boutin S (2000) The determinants of optimal litter size in free-ranging red squirrels. Ecology 81:2867–2877
Kerr TD, Boutin S, LaMontagne JM, McAdam AG, Humphries MM (2007) Persistent maternal effects on juvenile survival in North American red squirrels. Biol Lett 3:289–291. https://doi.org/10.1098/rsbl.2006.0615
Klug H, Bonsall MB (2014) What are the benefits of parental care? The importance of parental effects on developmental rate. Ecol Evol 4:2330–2351. https://doi.org/10.1002/ece3.1083
Kuznetsova A, Brockhoff P, Christensen R (2016) lmerTest: tests in linear mixed effects models. R package version 3.0.0, https://cran.r-project.org/package=lmerTest. Accessed 15 Feb 2019
Lailvaux SP, Kasumovic MM (2011) Defining individual quality over lifetimes and selective contexts. Proc R Soc Lond B 278:321–328. https://doi.org/10.1098/rspb.2010.1591
LaMontagne JM, Boutin S (2007) Local-scale synchrony and variability in mast seed production patterns of Picea glauca. J Ecol 95:991–1000. https://doi.org/10.1111/j.1365-2745.2007.01266.x
LaMontagne JM, Peters S, Boutin S (2005) A visual index for estimating cone production for individual white spruce trees. Can J For Res 35:3020–3026. https://doi.org/10.1139/x05-210
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
Maestripieri D, Mateo J (2009) The role of maternal effects in mammalian evolution and adaptation. In: Maestripieri D, Mateo J (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 1–10
Mann PE (1993) Measurement of maternal behavior. Methods Neurosci 14:343–358
Martinig AR, McAdam AG, Dantzer B, Lane JE, Coltman DW, Boutin S (2020) The new kid on the block: immigrant males win big whereas females pay fitness cost after dispersal. Ecol Lett 23:430–438. https://doi.org/10.1111/ele.13436
Martins T, Roberts M, Giblin I, Huxham R, Evans M (2007) Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches. Horm Behav 52:445–453. https://doi.org/10.1016/j.yhbeh.2007.06.007
McAdam AG, Boutin S (2003a) Variation in viability selection among cohorts of juvenile red squirrels (Tamiasciurus hudsonicus). Evolution 57:1689–1697. https://doi.org/10.1111/j.0014-3820.2003.tb00374.x
McAdam AG, Boutin S (2003b) Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels. J Evol Biol 16:1249–1256. https://doi.org/10.1046/j.1420-9101.2003.00630.x
McAdam AG, Boutin S, Dantzer B, Lane JE (2019) Seed masting causes fluctuations in optimum litter size and lag load in a seed predator. Am Nat 194:574–589. https://doi.org/10.1086/703743
McAdam AG, Boutin S, Réale D, Berteaux D (2002) Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846–851
McAdam AG, Boutin S, Sykes AK, Humphries MM (2007) Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Ecoscience 14:362–369. https://doi.org/10.2980/1195-6860(2007)14[362:LHOFRS]2.0.CO;2
Nice MM, Nice C, Ewers D (1956) Comparison of behavior development in snowshoe hares and red squirrels. J Mammal 37:64–74. https://doi.org/10.2307/1375527
Nienstaedt H, Zasada JC (1990) Picea glauca. In: Burns RM, Honkala BH (eds) Silvics of North America, vol 1. USDA Forest Service, Washington, pp 204–226
Numan M, Insel TR (2006) The neurobiology of parental care, vol 1. Springer Science & Buisness Media, New York
Numan M, Woodside B (2010) Maternity: neural mechanisms motivational processes, and physiological adaptations. Behav Neurosci 124:715–741. https://doi.org/10.1037/a0021548
Olazábal DE, Pereira M, Agrati D, Ferreira A, Fleming AS, González-Mariscal G, Lévy F, Lucion AB, Morrell JI, Numan M, Uriarte N (2013) New theoretical and experimental approaches on maternal motivation in mammals. Neurosci Biobehav Res 37:1860–1874. https://doi.org/10.1016/j.neubiorev.2013.04.003
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reinhold K (2002) Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J Hered 93:400–405. https://doi.org/10.1093/jhered/93.6.400
Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425. https://doi.org/10.1016/S0169-5347(00)01941-8
Roff D (1998) The detection and measurement of maternal effects. In: Mousseau T, Fox C (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 83–96
Rogowitz GL (1996) Trade-offs in energy allocation during lactation. Am Zool 36:197–204. https://doi.org/10.1093/icb/36.2.197
Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, Oxford
Schradin C, Anzenberger G (2001) Infant carrying in family groups of Goeldi’s monkeys (Callimico goeldii). Am J Primatol 53:57–67
Seip KM, Morrell JI (2008) Exposure to pups influences the strength of maternal motivation in virgin female rats. Physiol Behav 95:599–608. https://doi.org/10.1016/j.physbeh.2008.09.003
Siracusa ER, Morandini M, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2017) Red squirrel territorial vocalizations deter intrusions by conspecific rivals. Behaviour 154:1259–1273. https://doi.org/10.1163/1568539X-00003467
Siracusa ER, Wilson DR, Studd EK, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2019) North American red squirrels mitigate costs of territory defense through social plasticity. Anim Behav 151:29–42. https://doi.org/10.1016/j.anbehav.2019.02.014
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506. https://doi.org/10.1086/282929
Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268
Stewart FEC, McAdam AG (2014) Seasonal plasticity of maternal behaviour in Peromyscus maniculatus. Behaviour 151:1641–1662. https://doi.org/10.1163/1568539X-00003211
Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644. https://doi.org/10.1111/2041-210X.12797
Streubel DP (1968) Food storing and related behavior of red squirrels (Tamiasciurus hudsonicus) in interior Alaska. MSc thesis, University of Alaska
Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC, Coltman DW, McAdam AG (2012) Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. J Evol Biol 25:614–624. https://doi.org/10.1111/j.1420-9101.2012.02456.x
Taylor RW, Boutin S, Humphries MM, McAdam AG (2014) Selection on female behaviour fluctuates with offspring environment. J Evol Biol 27:2308–2321. https://doi.org/10.1111/jeb.12495
Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264. https://doi.org/10.1093/icb/14.1.249
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142. https://doi.org/10.1086/284547
van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73. https://doi.org/10.1098/rspb.2003.2518
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Wartella J, Amory E, Macbeth A, McNamara I, Stevens L, Lambert KG, Kinsley CH (2003) Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat. Physiol Behav 79:373–381. https://doi.org/10.1016/S0031-9384(03)00150-1
Williams CT, Lane JE, Humphries MM, McAdam AG, Boutin S (2014) Reproductive phenology of a food-hoarding mast-seed consumer: resource- and density-dependent benefits of early breeding in red squirrels. Oecologia 174:777–788. https://doi.org/10.1007/s00442-013-2826-1
Wilson ADM, Krause J (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323. https://doi.org/10.1093/beheco/ars123
Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214. https://doi.org/10.1016/j.tree.2009.10.002
Zhong M, Hess KR (2009) Mean survival time from right censored data. COBRA Preprint Series 66, https://core.ac.uk/download/pdf/61320547.pdf. Accessed 21 Oct 2019
Acknowledgments
We thank Agnes MacDonald and her family for long-term access to her trapline, and Champagne and Aishihik First Nations for allowing us to conduct our work within their traditional territory. We thank all volunteers, field assistants, and graduate students for their assistance in data collection. We thank two anonymous reviewers for their constructive feedback that improved this manuscript. This is publication #109 of the Kluane Red Squirrel Project.
Funding
This study was funded by American Society of Mammalogists to SEW; University of Michigan to SEW and BD; National Science Foundation (IOS-1749627 to BD, DEB-0515849 to AGM); and Natural Sciences and Engineering Research Council to SB, AGM, and JEL.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All work was conducted under animal ethics approvals from Michigan State University (AUF#04/08-046-00), University of Guelph (AUP#09R006), and University of Michigan (PRO00005866).
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Communicated by A. I Schulte-Hostedde
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Westrick, S.E., Taylor, R.W., Boutin, S. et al. Attentive red squirrel mothers have faster growing pups and higher lifetime reproductive success. Behav Ecol Sociobiol 74, 72 (2020). https://doi.org/10.1007/s00265-020-02856-7
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DOI: https://doi.org/10.1007/s00265-020-02856-7