Advertisement

Allomaternal care, brains and fertility in mammals: who cares matters

  • Sandra A. HeldstabEmail author
  • Karin Isler
  • Judith M. Burkart
  • Carel P. van Schaik
Original Article

Abstract

The expensive brain hypothesis predicts that the lowest stable level of energy input sets the upper limit to a species’ brain size. This prediction receives comparative support from the effects of experienced seasonality (including hibernation) and diet quality on mammalian brain size. Here, we test another prediction, which concerns the temporal stability of energy inputs. Allomaternal care in mammals can be provided by breeding males or other helpers (usually earlier offspring). Male care should be stable and reliable since otherwise no breeding would occur. Care by others, in contrast, should fluctuate, as the availability of helpers often varies. One would therefore predict, other things being equal, that the presence of male care in addition to maternal care should show positive correlated evolution with brain size, whereas care by others would not. However, because females can readily respond through litter size adjustments to variable amounts of energy inputs, helper inputs may be used to increase fertility. A detailed comparative analysis of a large sample of mammals (N = 478 species) showed that male help is correlated with the evolution of larger brains, whereas alloparental help is correlated with higher fertility, but only in species where male care is also present (as in cooperative breeders). Humans evolved an unusual form of multi-family cooperative breeding, which involves stable and reliable care by both fathers and alloparents. This combination helps to explain why humans differ from the other apes in having both an extremely large brain and a relatively high reproductive output.

Significance statement

Allomaternal care provides breeding females with energy, directly or indirectly, and so would be expected to affect fertility and/or brain size. Which path evolution actually took remains controversial, partly because previous studies did not separate between care provided by the breeding male (paternal care) and care by non-breeding helpers (alloparental care). We distinguish between them because we expect that selection only favours increased brain size if the increase in energy available to the female is predictable and constant. Using a sample of 478 mammals, we show that paternal care, which is both reliable and stable, shows correlated evolution with brain size, whereas alloparental care, which fluctuates with varying availability of helpers, is correlated with higher fertility. Thus, constraints on brain size, imposed by its high-energy costs, may predict brain size better than the fitness benefits of improved cognitive abilities per se.

Keywords

Allomaternal care Paternal care Cooperative breeding Brain size Fertility Reproduction 

Notes

Acknowledgments

We are thankful to the editor and the two anonymous reviewers for their constructive and thoughtful comments on previous versions of the manuscript.

Funding

Financial support was provided by the Swiss National Science Foundation grant no. 31003A-144210, the A.H. Schultz Foundation and the University of Zurich.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical statement

All sources of data were from the literature or the web and did not involve ethical approval.

Data availability

The dataset and all additional analyses supporting the conclusions of this article are available in this published article and in the supplementary information files.

Supplementary material

265_2019_2684_MOESM1_ESM.xlsx (80 kb)
ESM 1 (XLSX 80.2 kb)
265_2019_2684_MOESM2_ESM.pdf (502 kb)
ESM 2 (PDF 501  kb)
265_2019_2684_MOESM3_ESM.docx (124 kb)
ESM 3 (DOCX 123 kb)
265_2019_2684_MOESM4_ESM.pdf (239 kb)
ESM 4 (PDF 239 kb)

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723.  https://doi.org/10.1109/TAC.1974.1100705 CrossRefGoogle Scholar
  2. Arlet ME, Isbell LA, Kaasik A, Molleman F, Chancellor RL, Chapman CA, Mänd R, Carey JR (2015) Determinants of reproductive performance among female gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. Int J Primatol 36:55–73.  https://doi.org/10.1109/TAC.1974.1100705 CrossRefGoogle Scholar
  3. Baldovino MC, Di Bitetti MS (2008) Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier? Folia Primatol 79:79–92.  https://doi.org/10.1159/000108780 CrossRefPubMedGoogle Scholar
  4. Bales K, Dietz J, Baker A, Miller K, Tardif SD (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71:27–38.  https://doi.org/10.1159/000021728 CrossRefPubMedGoogle Scholar
  5. Barrett L, Henzi P (2005) The social nature of primate cognition. Proc R Soc Lond B 272:1865–1875.  https://doi.org/10.1098/rspb.2005.3200 CrossRefGoogle Scholar
  6. Barton RA, Capellini I (2011) Maternal investment, life histories, and the costs of brain growth in mammals. P Natl Acad Sci USA 108:6169–6174.  https://doi.org/10.1073/pnas.1019140108 CrossRefGoogle Scholar
  7. Bauernfeind AL, Barks SK, Duka T, Grossman LI, Hof PR, Sherwood CC (2014) Aerobic glycolysis in the primate brain: reconsidering the implications for growth and maintenance. Brain Struct Funct 219:1149–1167.  https://doi.org/10.1007/s00429-013-0662-z CrossRefPubMedGoogle Scholar
  8. Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality. Cambridge University Press, CambridgeGoogle Scholar
  9. Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE (2016) Brain size predicts problem-solving ability in mammalian carnivores. P Natl Acad Sci USA 113:2532–2537.  https://doi.org/10.1073/pnas.1505913113 CrossRefGoogle Scholar
  10. Bernard RTF, Nurton J (1993) Ecological correlates of relative brain size in some South-African rodents. S Afr J Zool 28:95–98.  https://doi.org/10.1080/02541858.1993.11448300 CrossRefGoogle Scholar
  11. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512.  https://doi.org/10.1038/nature05634 CrossRefPubMedGoogle Scholar
  12. Borrego N, Gaines M (2016) Social carnivores outperform asocial carnivores on an innovative problem. Anim Behav 114:21–26.  https://doi.org/10.1016/j.anbehav.2016.01.013 CrossRefGoogle Scholar
  13. Bourlière F (1970) Ecology and behaviour of Lowe’s guenon (Cercopithecus campbelli lowei) in the Ivory Coast. In: Napier JR, Napier PH (eds) Old World monkeys: evolution, systematics and behaviour. Academic Press, New York, pp 297–350Google Scholar
  14. Brouwer L, van de Pol M, Atema E, Cockburn A (2011) Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric. Mol Ecol 20:4796–4807.  https://doi.org/10.1111/j.1365-294X.2011.05325.x CrossRefPubMedGoogle Scholar
  15. Browning RC, Baker EA, Herron JA, Kram R (2006) Effects of obesity and sex on the energetic cost and preferred speed of walking. J Appl Physiol 100:390–398.  https://doi.org/10.1152/japplphysiol.00767.2005 CrossRefPubMedGoogle Scholar
  16. Burkart JM, van Schaik CP (2010) Cognitive consequences of cooperative breeding in primates? Anim Cogn 13:1–19.  https://doi.org/10.1007/s10071-009-0263-7 CrossRefPubMedGoogle Scholar
  17. Burkart JM, Hrdy SB, van Schaik CP (2009) Cooperative breeding and human cognitive evolution. Evol Anthropol 18:175–186.  https://doi.org/10.1002/evan.20222 CrossRefGoogle Scholar
  18. Burkart JM, Schubiger MN, van Schaik CP (2016) The evolution of general intelligence. Behav Brain Sci 40:1–65.  https://doi.org/10.1017/S0140525X16000959 CrossRefGoogle Scholar
  19. Butte NF, King JC (2005) Energy requirements during pregnancy and lactation. Public Health Nutr 8:1010–1027.  https://doi.org/10.1079/PHN2005793 CrossRefPubMedGoogle Scholar
  20. Byrne RW, Whiten A (1988) Machiavellian intelligence. Social expertise and the evolution of intellect in monkeys, apes, and humans. Clarendon Press, OxfordGoogle Scholar
  21. Clutton-Brock T, Harvey PH (1980) Primates, brains and ecology. J Zool 190:309–323.  https://doi.org/10.1111/j.1469-7998.1980.tb01430.x CrossRefGoogle Scholar
  22. Clutton-Brock T, Russell A, Sharpe L, Young A, Balmforth Z, McIlrath G (2002) Evolution and development of sex differences in cooperative behavior in meerkats. Science 297:253–256.  https://doi.org/10.1126/science.1071412 CrossRefPubMedGoogle Scholar
  23. Clutton-Brock T, Russell A, Sharpe L (2004) Behavioural tactics of breeders in cooperative meerkats. Anim Behav 68:1029–1040.  https://doi.org/10.1016/j.anbehav.2003.10.024 CrossRefGoogle Scholar
  24. Creel S, Creel NM (2002) The African wild dog: behavior, ecology, and conservation. Princeton University Press, PrincetonGoogle Scholar
  25. Deaner RO, Isler K, Burkart J, van Schaik C (2007) Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav Evol 70:115–124.  https://doi.org/10.1159/000102973 CrossRefPubMedGoogle Scholar
  26. DeCasien AR, Williams SA, Higham JP (2017) Primate brain size is predicted by diet but not sociality. Nat Ecol Evol 1:112.  https://doi.org/10.1038/s41559-017-0112 CrossRefPubMedGoogle Scholar
  27. Dixit T, English S, Lukas D (2017) The relationship between egg size and helper number in cooperative breeders: a meta-analysis across species. PeerJ 5:e4028.  https://doi.org/10.7717/peerj.4028 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46.  https://doi.org/10.1111/j.1600-0587.2012.07348.x CrossRefGoogle Scholar
  29. Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347.  https://doi.org/10.1126/science.1145463 CrossRefPubMedGoogle Scholar
  30. Dunbar RIM, Shultz S (2017) Why are there so many explanations for primate brain evolution? Philos Trans R Soc B 372:20160244.  https://doi.org/10.1098/rstb.2016.0244 CrossRefGoogle Scholar
  31. Dyble M, Thompson J, Smith D, Salali GD, Chaudhary N, Page AE, Vinicuis L, Mace R, Migliano AB (2016) Networks of food sharing reveal the functional significance of multilevel sociality in two hunter-gatherer groups. Curr Biol 26:2017–2021.  https://doi.org/10.1016/j.cub.2016.05.064 CrossRefPubMedGoogle Scholar
  32. Emery NJ, Seed AM, von Bayern AM, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Philos Trans R Soc B 362:489–505.  https://doi.org/10.1098/rstb.2006.1991 CrossRefGoogle Scholar
  33. Emlen ST, Wrege PH (1991) Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. J Anim Ecol 60:309–326.  https://doi.org/10.2307/5462 CrossRefGoogle Scholar
  34. Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 40:553–562.  https://doi.org/10.1016/S0003-3472(05)80536-6 CrossRefGoogle Scholar
  35. Fernandes HBF, Woodley MA, Nijenhuis JT (2014) Differences in cognitive abilities among primates are concentrated on G: phenotypic and phylogenetic comparisons with two meta-analytical databases. Intelligence 46:311–322.  https://doi.org/10.1016/j.intell.2014.07.007 CrossRefGoogle Scholar
  36. Fish JL, Lockwood CA (2003) Dietary constraints on encephalization in primates. Am J Phys Anthropol 120:171–181.  https://doi.org/10.1002/ajpa.10136 CrossRefPubMedGoogle Scholar
  37. Fox J, Weisberg S (2011) An {R} companion to applied regression, vol 2. Sage, Thousand OaksGoogle Scholar
  38. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726.  https://doi.org/10.1086/343873 CrossRefPubMedGoogle Scholar
  39. Fritz SA, Bininda-Emonds ORP, Purvis A (2009) Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol Lett 12:538–549.  https://doi.org/10.1111/j.1461-0248.2009.01307.x CrossRefPubMedGoogle Scholar
  40. Garamszegi LZ, Mundry R (2014) Multimodel-inference in comparative analyses. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin, pp 305–331CrossRefGoogle Scholar
  41. Garber PA, Leigh SR (1997) Ontogenetic variation in small-bodied new world primates: implications for patterns of reproduction and infant care. Folia Primatol 68:1–22.  https://doi.org/10.1159/000157226 CrossRefPubMedGoogle Scholar
  42. Gartlan J (1969) Sexual and maternal behavior of the vervet monkey, Cercopithecus aethiops. J Reprod Fertil 6:137–150Google Scholar
  43. Genoud M, Isler K, Martin RD (2018) Comparative analyses of basal rate of metabolism in mammals: data selection does matter. Biol Rev 93:404–438.  https://doi.org/10.1111/brv.12350 CrossRefPubMedGoogle Scholar
  44. Gilchrist JS, Russell AF (2007) Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (Mungos mungo). Behav Ecol Sociobiol 61:1053–1060.  https://doi.org/10.1007/s00265-006-0338-2 CrossRefGoogle Scholar
  45. Gittleman JL (1986) Carnivore brain size, behavioral ecology, and phylogeny. J Mammal 67:23–36.  https://doi.org/10.2307/1380998 CrossRefGoogle Scholar
  46. Gittleman JL (1989) Carnivore group living: comparative trends. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Springer, Berlin, pp 183–207CrossRefGoogle Scholar
  47. Grueber C, Nakagawa S, Laws R, Jamieson I (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711.  https://doi.org/10.1111/j.1420-9101.2010.02210.x CrossRefGoogle Scholar
  48. Gubernick DJ, Laskin B (1994) Mechanisms influencing sibling care in the monogamous biparental California mouse, Peromyscus californicus. Anim Behav 48:1235–1237.  https://doi.org/10.1006/anbe.1994.1356 CrossRefGoogle Scholar
  49. Gurven M (2004) To give and to give not: the behavioral ecology of human food transfers. Behav Brain Sci 27:543–559.  https://doi.org/10.1017/S0140525X04000123 CrossRefGoogle Scholar
  50. Haber GC (1977) Socio-ecological dynamics of wolves and prey in a subarctic ecosystem. PhD dissertation, University of British ColumbiaGoogle Scholar
  51. Hair J, Black W, Babin B, Anderson R, Tatham R (2006) Multivariate data analysis. Pearson Prentice Hall, Upper Saddle RiverGoogle Scholar
  52. Harrington FH, Mech LD, Fritts SH (1983) Pack size and wolf pup survival: their relationship under varying ecological conditions. Behav Ecol Sociobiol 13:19–26.  https://doi.org/10.1007/BF00295072 CrossRefGoogle Scholar
  53. Harvey PH, Clutton-Brock T, Mace GM (1980) Brain size and ecology in small mammals and primates. P Natl Acad Sci USA 77:4387–4389.  https://doi.org/10.1073/pnas.77.7.4387 CrossRefGoogle Scholar
  54. Hawkes K, O’Connell JF, Jones NB, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. P Natl Acad Sci USA 95:1336–1339.  https://doi.org/10.1073/pnas.95.3.1336 CrossRefGoogle Scholar
  55. Heesen M, Rogahn S, Ostner J, Schülke O (2013) Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67:1053–1066.  https://doi.org/10.1007/s00265-013-1530-9 CrossRefGoogle Scholar
  56. Heinsohn R, Cockburn A (1994) Helping is costly to young birds in cooperatively breeding white-winged choughs. Proc R Soc Lond B 256:293–298.  https://doi.org/10.1098/rspb.1994.0083 CrossRefGoogle Scholar
  57. Heldstab SA, van Schaik CP, Isler K (2016a) Being fat and smart: a comparative analysis of the fat-brain trade-off in mammals. J Hum Evol 100:25–34.  https://doi.org/10.1016/j.jhevol.2016.09.001 CrossRefGoogle Scholar
  58. Heldstab SA, Kosonen ZK, Koski S, Burkart JM, van Schaik CP, Isler K (2016b) Manipulation complexity in primates coevolved with brain size and terrestriality. Sci Rep 6:24528.  https://doi.org/10.1038/srep24528 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Heldstab SA, van Schaik CP, Isler K (2017) Getting fat or getting help? How female mammals cope with energetic constraints on reproduction. Front Zool 14:29.  https://doi.org/10.1186/s12983-017-0214-0
  60. Heldstab SA, Müller DWH, Graber SM, Bingaman Lackey L, Rensch E, Hatt J-M, Zerbe P, Clauss M (2018a) Geographical origin, delayed implantation and induced ovulation explain reproductive seasonality in carnivores. J Biol Rhythms 33:402–419.  https://doi.org/10.1177/0748730418773620 CrossRefGoogle Scholar
  61. Heldstab SA, Isler K, van Schaik CP (2018b) Hibernation constrains brain size evolution in mammals. J Evol Biol 31:1582–1588.  https://doi.org/10.1111/jeb.13353 CrossRefPubMedGoogle Scholar
  62. Hewlett BS (1993) Intimate fathers: the nature and context of Aka Pygmy paternal infant care. University of Michigan Press, Ann ArborGoogle Scholar
  63. Hill K, Hurtado AM (2009) Cooperative breeding in South American hunter–gatherers. Proc R Soc Lond B 276:3863–3870.  https://doi.org/10.1098/rspb.2009.1061 CrossRefGoogle Scholar
  64. Hill K, Kaplan H, Hawkes K (1993) On why male foragers hunt and share food. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  65. Holliday MA (1986) Body composition and energy needs during growth. In: Falkner F, Tanner JM (eds) Postnatal growth neurobiology, vol 2. Springer, New York, pp 101–117CrossRefGoogle Scholar
  66. Hrdy SB (1976) Care and exploitation of nonhuman primate infants by conspecifics other than the mother. Adv Study Behav 6:101–158.  https://doi.org/10.1016/S0065-3454(08)60083-2 CrossRefGoogle Scholar
  67. Hrdy SB (2005) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Anhert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis. MIT Press, Cambridge, pp 9–32Google Scholar
  68. Hrdy SB (2009) Mothers and others: the evolutionary origins of mutual understanding. Harvard University Press, CambridgeGoogle Scholar
  69. Isler K, van Schaik CP (2006a) Metabolic costs of brain size evolution. Biol Lett 2:557–560.  https://doi.org/10.1098/rsbl.2006.0538 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Isler K, van Schaik C (2006b) Costs of encephalization: the energy trade-off hypothesis tested on birds. J Hum Evol 51:228–243.  https://doi.org/10.1016/j.jhevol.2006.03.006 CrossRefPubMedGoogle Scholar
  71. Isler K, van Schaik CP (2009a) The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol 57:392–400.  https://doi.org/10.1016/j.jhevol.2009.04.009 CrossRefPubMedGoogle Scholar
  72. Isler K, van Schaik CP (2009b) Why are there so few smart mammals (but so many smart birds)? Biol Lett 5:125–129.  https://doi.org/10.1098/rsbl.2008.0469 CrossRefPubMedGoogle Scholar
  73. Isler K, van Schaik CP (2012) Allomaternal care, life history and brain size evolution in mammals. J Hum Evol 63:52–63.  https://doi.org/10.1016/j.jhevol.2012.03.009 CrossRefPubMedGoogle Scholar
  74. Isler K, Kirk EC, Miller JM, Albrecht GA, Gelvin BR, Martin RD (2008) Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J Hum Evol 55:967–978.  https://doi.org/10.1016/j.jhevol.2008.08.004 CrossRefPubMedGoogle Scholar
  75. Iwaniuk AN, Arnold KE (2004) Is cooperative breeding associated with bigger brains? A comparative test in the Corvida (Passeriformes). Ethology 110:203–220.  https://doi.org/10.1111/j.1439-0310.2003.00957.x CrossRefGoogle Scholar
  76. Jaeggi AV, Hooper PL, Beheim BA, Kaplan H, Gurven M (2016) Reciprocal exchange patterned by market forces helps explain cooperation in a small-scale society. Curr Biol 26:2180–2187.  https://doi.org/10.1016/j.cub.2016.06.019 CrossRefPubMedGoogle Scholar
  77. Jaquish C, Tardif S, Cheverud J (1997) Interactions between infant growth and survival: evidence for selection on age-specific body weight in captive common marmosets (Callithrix jacchus). Am J Primatol 42:269–280.  https://doi.org/10.1002/(SICI)1098-2345(1997)42:4<269::AID-AJP2>3.0.CO;2-V CrossRefPubMedGoogle Scholar
  78. Jerison HJ (1973) Evolution of the brain and intelligence. Academic Press, New YorkGoogle Scholar
  79. Jones KE, Bielby J, Cardillo M, Fritz SA, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster CA, Price SA, Rigby EA, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648–2648.  https://doi.org/10.1890/08-1494.1 CrossRefGoogle Scholar
  80. Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185.  https://doi.org/10.1002/1520-6505(2000)9:4<156::AID-EVAN5>3.0.CO;2-7 CrossRefGoogle Scholar
  81. Kirk EC (2006) Visual influences on primate encephalization. J Hum Evol 51:76–90.  https://doi.org/10.1016/j.jhevol.2006.01.005 CrossRefPubMedGoogle Scholar
  82. Klauke N, Segelbacher G, Schaefer H (2013) Reproductive success depends on the quality of helpers in the endangered, cooperative El Oro parakeet (Pyrrhura orcesi). Mol Ecol 22:2011–2027.  https://doi.org/10.1111/mec.12219 CrossRefPubMedGoogle Scholar
  83. Koenig A (1995) Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus). Am J Primatol 35:311–317.  https://doi.org/10.1002/ajp.1350350407 CrossRefGoogle Scholar
  84. Komdeur J (1994) Experimental evidence for helping and hindering by previous offspring in the cooperative-breeding Seychelles warbler Acrocephalus sechellensis. Behav Ecol Sociobiol 34:175–186.  https://doi.org/10.1007/BF00167742 CrossRefGoogle Scholar
  85. Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brännström I, Immler S, Maklakov AA, Kolm N (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171.  https://doi.org/10.1016/j.cub.2012.11.058 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Kuzawa CW, Chugani HT, Grossman LI, Lipovich L, Muzik O, Hof PR, Wildman DE, Sherwood CC, Leonard WR, Lange N (2014) Metabolic costs and evolutionary implications of human brain development. P Natl Acad Sci USA 111:13010–13015.  https://doi.org/10.1073/pnas.1323099111 CrossRefGoogle Scholar
  87. Kuznetsova TA, Kam M, Khokhlova IS, Kostina NV, Dobrovolskaya TG, Umarov MM, Degen AA, Shenbrot GI, Krasnov BR (2013) Desert gerbils affect bacterial composition of soil. Microb Ecol 66:940–949.  https://doi.org/10.1007/s00248-013-0263-7 CrossRefPubMedGoogle Scholar
  88. Lancaster JB (1971) Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol 15:161–182.  https://doi.org/10.1159/000155377 CrossRefGoogle Scholar
  89. Legge S (2000) Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav 59:1009–1018.  https://doi.org/10.1006/anbe.2000.1382 CrossRefPubMedGoogle Scholar
  90. Lonstein JS, De Vries GJ (2000) Influence of gonadal hormones on the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behav Brain Res 114:79–87.  https://doi.org/10.1016/S0166-4328(00)00192-3 CrossRefPubMedGoogle Scholar
  91. Lonstein JS, De Vries GJ (2001) Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster). J Comp Physiol 115:53–61.  https://doi.org/10.1037//0735-7036.115.1.53 CrossRefGoogle Scholar
  92. Lovegrove BG, Lobban KD, Levesque DL (2014) Mammal survival at the Cretaceous–Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs. Proc R Soc Lond B 281:20141304.  https://doi.org/10.1098/rspb.2014.1304 CrossRefGoogle Scholar
  93. Lukas WD, Campbell BC (2000) Evolutionary and ecological aspects of early brain malnutrition in humans. Hum Nat 11:1–26.  https://doi.org/10.1007/s12110-000-1000-8 CrossRefPubMedGoogle Scholar
  94. Lukas D, Clutton-Brock T (2012) Life histories and the evolution of cooperative breeding in mammals. Proc R Soc Lond B 279:4065–4070.  https://doi.org/10.1098/rspb.2012.1433 CrossRefGoogle Scholar
  95. Lukas D, Clutton-Brock TH (2013) The evolution of social monogamy in mammals. Science 341:526–530.  https://doi.org/10.1126/science.1238677 CrossRefPubMedGoogle Scholar
  96. Luo Y, Zhong MJ, Huang Y, Li F, Liao WB, Kotrschal A (2017) Seasonality and brain size are negatively associated in frogs: evidence for the expensive brain framework. Sci Rep 7:16629.  https://doi.org/10.1038/s41598-017-16921-1 CrossRefPubMedPubMedCentralGoogle Scholar
  97. MacColl AD, Hatchwell BJ (2003) Sharing of caring: nestling provisioning behaviour of long-tailed tit, Aegithalos caudatus, parents and helpers. Anim Behav 66:955–964.  https://doi.org/10.1006/anbe.2003.2268 CrossRefGoogle Scholar
  98. Macdonald DW, Moehlman PD (1982) Cooperation, altruism, and restraint in the reproduction of carnivores. In: Bateson PPGKP (ed) Perspectives in ethology, vol 5. Plenum Press, New York, pp 433–467Google Scholar
  99. MacLeod KJ, McGhee KE, Clutton-Brock TH (2015) No apparent benefits of allonursing for recipient offspring and mothers in the cooperatively breeding meerkat. J Anim Ecol 84:1050–1058.  https://doi.org/10.1111/1365-2656.12343 CrossRefPubMedGoogle Scholar
  100. Maestripieri D (1994) Social structure, infant handling, and mothering styles in group-living Old World monkeys. Int J Primatol 15:531–553.  https://doi.org/10.1007/BF02735970 CrossRefGoogle Scholar
  101. Malcolm JR, Marten K (1982) Natural selection and the communal rearing of pups in African wild dogs (Lycaon pictus). Behav Ecol Sociobiol 10:1–13.  https://doi.org/10.1007/BF00296390 CrossRefGoogle Scholar
  102. Marlowe F (1999) Male care and mating effort among Hadza foragers. Behav Ecol Sociobiol 46:57–64.  https://doi.org/10.1007/s002650050592 CrossRefGoogle Scholar
  103. Marlowe F (2000) Paternal investment and the human mating system. Behav Process 51:45–61.  https://doi.org/10.1016/S0376-6357(00)00118-2 CrossRefGoogle Scholar
  104. Marshall HH, Sanderson JL, Mwanghuya F, Businge R, Kyabulima S, Hares MC, Inzani E, Kalema-Zikusoka G, Mwesige K, Thompson FJ (2016) Variable ecological conditions promote male helping by changing banded mongoose group composition. Behav Ecol 27:978–987.  https://doi.org/10.1093/beheco/arw006 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Matějů J, Kratochvíl L, Pavelková Z, Řičánková VP, Vohralík V, Němec P (2016) Absolute, not relative brain size correlates with sociality in ground squirrels. Proc R Soc Lond B 283:20152725.  https://doi.org/10.1098/rspb.2015.2725 CrossRefGoogle Scholar
  106. McNab BK (2006) The energetics of reproduction in endotherms and its implication for their conservation. Integr Comp Biol 46:1159–1168.  https://doi.org/10.1093/icb/icl016 CrossRefPubMedGoogle Scholar
  107. Mink JW, Blumenschine RJ, Adams DB (1981) Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis. Am J Phys 241:R203–R212.  https://doi.org/10.1152/ajpregu.1981.241.3.R203 CrossRefGoogle Scholar
  108. Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40:213–220.  https://doi.org/10.1007/s002650050335 CrossRefGoogle Scholar
  109. Moehlman PD (1979) Jackal helpers and pup survival. Nature 277:382–383.  https://doi.org/10.1038/277382a0 CrossRefGoogle Scholar
  110. Moehlman PD, Hofer H (1997) Cooperative breeding, reproductive suppression, and body mass in canids. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 76–127Google Scholar
  111. Mumme RL (1992) Do helpers increase reproductive success? Behav Ecol Sociobiol 31:319–328.  https://doi.org/10.1007/BF00177772 CrossRefGoogle Scholar
  112. Murie A (2011) The wolves of Mount McKinley. University of Washington Press, SeattleGoogle Scholar
  113. Myers P, Espinosa R, Parr C, Jones T, Hammond G, Dewey T (2006) The animal diversity web, http://animaldiversity.ummz.umich.edu/
  114. Navarrete A, van Schaik CP, Isler K (2011) Energetics and the evolution of human brain size. Nature 480:91–94.  https://doi.org/10.1038/nature10629 CrossRefPubMedGoogle Scholar
  115. Navarrete AF, Reader SM, Street SE, Whalen A, Laland KN (2016) The coevolution of innovation and technical intelligence in primates. Philos Trans R Soc B 371:20150186.  https://doi.org/10.1098/rstb.2015.0186 CrossRefGoogle Scholar
  116. Nichols HJ, Amos W, Bell MB, Mwanguhya F, Kyabulima S, Cant MA (2012) Food availability shapes patterns of helping effort in a cooperative mongoose. Anim Behav 83:1377–1385.  https://doi.org/10.1016/j.anbehav.2012.03.005 CrossRefGoogle Scholar
  117. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804.  https://doi.org/10.1242/jeb.017574 CrossRefPubMedGoogle Scholar
  118. Orme D (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R package version 0.5.2, http://CRAN.R-project.org/package=caper
  119. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884.  https://doi.org/10.1038/44766 CrossRefPubMedGoogle Scholar
  120. Parker ST, Gibson KR (1977) Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J Hum Evol 6:623–641.  https://doi.org/10.1016/S0047-2484(77)80135-8 CrossRefGoogle Scholar
  121. Pérez-Barbería FJ, Gordon IJ (2005) Gregariousness increases brain size in ungulates. Oecologia 145:41–52.  https://doi.org/10.1007/s00442-005-0067-7 CrossRefPubMedGoogle Scholar
  122. Powell LE, Isler K, Barton RA (2017) Re-evaluating the link between brain size and behavioural ecology in primates. Proc R Soc Lond B 284:20171765.  https://doi.org/10.1098/rspb.2017.1765 CrossRefGoogle Scholar
  123. Price EC (1992) The benefits of helpers: effects of group and litter size on infant care in tamarins (Saguinus oedipus). Am J Primatol 26:179–190.  https://doi.org/10.1002/ajp.1350260304 CrossRefGoogle Scholar
  124. Quinlan RJ (2007) Human parental effort and environmental risk. Proc R Soc Lond B 274:121–125.  https://doi.org/10.1098/rspb.2006.3690 CrossRefGoogle Scholar
  125. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  126. R Core Team (2017) R: a language and environment for statistical computing. version 3.4.1. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/
  127. Reader SM, Hager Y, Laland KN (2011) The evolution of primate general and cultural intelligence. Philos Trans R Soc B 366:1017–1027.  https://doi.org/10.1098/rstb.2010.0342 CrossRefGoogle Scholar
  128. Reddon AR, O’Connor CM, Ligocki IY, Hellmann JK, Marsh-Rollo SE, Hamilton IM, Balshine S (2016) No evidence for larger brains in cooperatively breeding cichlid fishes. Can J Zool 94:373–378.  https://doi.org/10.1139/cjz-2015-0118 CrossRefGoogle Scholar
  129. Roberts RL, Miller AK, Taymans SE, Carter CS (1998) Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster). Can J Zool 76:1862–1868.  https://doi.org/10.1139/z98-156 CrossRefGoogle Scholar
  130. Rogerson P (2001) Statistical methods for geography, SageGoogle Scholar
  131. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758.  https://doi.org/10.1152/physrev.1997.77.3.731 CrossRefPubMedGoogle Scholar
  132. Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113.  https://doi.org/10.1159/000021733 CrossRefPubMedGoogle Scholar
  133. Rothe H, Darms K, Koenig A, Radespiel U, Juenemann B (1993) Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): effect of nonreproductive helpers on the parents’ carrying performance. Int J Primatol 14:79–93.  https://doi.org/10.1007/BF02196504 CrossRefGoogle Scholar
  134. Rowe N, Myers M (2011) All the world’s primates. Primate Conservation Inc., Charlestown http://www.alltheworldsprimates.org Google Scholar
  135. Russell EM (1974) Recent ecological studies on Australian marsupials. Austr Mammal 1:189–211.  https://doi.org/10.1007/978-94-017-6295-3_20 CrossRefGoogle Scholar
  136. Russell E, Rowley I (1988) Helper contributions to reproductive success in the splendid fairy-wren (Malurus splendens). Behav Ecol Sociobiol 22:131–140.  https://doi.org/10.1007/BF00303548 CrossRefGoogle Scholar
  137. Russell A, Brotherton P, McIlrath G, Sharpe L, Clutton-Brock T (2003) Breeding success in cooperative meerkats: effects of helper number and maternal state. Behav Ecol 14:486–492.  https://doi.org/10.1093/beheco/arg022 CrossRefGoogle Scholar
  138. Rymer TL, Pillay N (2014) Alloparental care in the African striped mouse Rhabdomys pumilio is age-dependent and influences the development of paternal care. Ethology 120:11–20.  https://doi.org/10.1111/eth.12175 CrossRefGoogle Scholar
  139. Santos CV, French JA, Otta E (1997) Infant carrying behavior in callitrichid primates: Callithrix and Leontopithecus. Int J Primatol 18:889–907.  https://doi.org/10.1023/A:1026340028851 CrossRefGoogle Scholar
  140. Santos MJ, Thorne JH, Moritz C (2015) Synchronicity in elevation range shifts among small mammals and vegetation over the last century is stronger for omnivores. Ecography 38:556–568.  https://doi.org/10.1111/ecog.00931 CrossRefGoogle Scholar
  141. SAS Institute Inc (1989–2016) JMP version 13.0. SAS Institute Inc., CaryGoogle Scholar
  142. Schubert M, Pillay N, Schradin C (2009) Parental and alloparental care in a polygynous mammal. J Mammal 90:724–731.  https://doi.org/10.1644/08-MAMM-A-175R1.1 CrossRefGoogle Scholar
  143. Sellen DW (2007) Evolution of infant and young child feeding: implications for contemporary public health. Annu Rev Nutr 27:123–148.  https://doi.org/10.1146/annurev.nutr.25.050304.092557 CrossRefPubMedGoogle Scholar
  144. Shultz S, Dunbar RIM (2007) The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc R Soc Lond B 274:2429–2436.  https://doi.org/10.1098/rspb.2007.0693 CrossRefGoogle Scholar
  145. Shultz S, Dunbar RIM (2010) Social bonds in birds are associated with brain size and contingent on the correlated evolution of life-history and increased parental investment. Biol J Linn Soc 100:111–123.  https://doi.org/10.1111/j.1095-8312.2010.01427.x CrossRefGoogle Scholar
  146. Siani JM (2009) Costs and benefits of cooperative infant care in wild golden lion tamarins (Leontopithecus rosalia). PhD dissertation, University of Maryland, College ParkGoogle Scholar
  147. Silk JB (1980) Kidnapping and female competition among captive bonnet macaques. Primates 21:100–110.  https://doi.org/10.1007/BF02383827 CrossRefGoogle Scholar
  148. Sol D (2009) The cognitive-buffer hypothesis for the evolution of large brains. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. Chicago University Press, Chicago, pp 111–134CrossRefGoogle Scholar
  149. Solomon NG (1991) Current indirect fitness benefits associated with philopatry in juvenile prairie voles. Behav Ecol Sociobiol 29:277–282.  https://doi.org/10.1007/BF00163985 CrossRefGoogle Scholar
  150. Sommer V (1989) Infant mistreatment in langur monkeys: sociobiology from the wrong end. In: Rasa A, Vogel C, Voland E (eds) The sociobiology of sexual and reproductive strategies. Chapman Hall, New York, pp 100–127Google Scholar
  151. Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc B 363:375–398.  https://doi.org/10.1098/rstb.2007.2145 CrossRefGoogle Scholar
  152. Stockley P, Hobson L (2016) Paternal care and litter size coevolution in mammals. Proc R Soc Lond B 283:20160140.  https://doi.org/10.1098/rspb.2016.0140 CrossRefGoogle Scholar
  153. Striedter GF (2005) Principles of brain evolution. Sinauer, SunderlandGoogle Scholar
  154. Symonds MR, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21.  https://doi.org/10.1007/s00265-010-1037-6 CrossRefGoogle Scholar
  155. Tardif SD, Carson RL, Gangaware BL (1992) Infant-care behavior of non-reproductive helpers in a communal-care primate, the cotton-top tamarin (Saguinus oedipus). Ethology 92:155–167.  https://doi.org/10.1111/j.1439-0310.1992.tb00956.x CrossRefGoogle Scholar
  156. Tibbetts EA (2007) Dispersal decisions and predispersal behavior in Polistes paper wasp ‘workers’. Behav Ecol Sociobiol 61:1877–1883.  https://doi.org/10.1007/s00265-007-0427-x CrossRefGoogle Scholar
  157. Tyler NJC (1987) Natural limitation of the abundance of the high arctic Svalbard reindeer. PhD dissertation, University of CambridgeGoogle Scholar
  158. van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130.  https://doi.org/10.1007/BF02557705 CrossRefPubMedGoogle Scholar
  159. van Schaik CP, Burkart JM (2010) Mind the gap: cooperative breeding and the evolution of our unique features. In: Kappeler PM, Silk J (eds) Mind the gap: tracing the origins of human universals. Springer, Berlin, pp 477–496CrossRefGoogle Scholar
  160. van Schaik CP, Burkart JM (2011) Social learning and evolution: the cultural intelligence hypothesis. Philos Trans R Soc B 366:1008–1016.  https://doi.org/10.1098/rstb.2010.0304 CrossRefGoogle Scholar
  161. van Woerden JT, van Schaik CP, Isler K (2010) Effects of seasonality on brain size evolution: evidence from strepsirrhine primates. Am Nat 176:758–767.  https://doi.org/10.1086/657045 CrossRefPubMedGoogle Scholar
  162. van Woerden JT, Willems EP, van Schaik CP, Isler K (2012) Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution 66:191–199.  https://doi.org/10.1111/j.1558-5646.2011.01434.x CrossRefPubMedGoogle Scholar
  163. van Woerden JT, van Schaik CP, Isler K (2014) Brief communication: seasonality of diet composition is related to brain size in new world monkeys. Am J Phys Anthropol 154:628–632.  https://doi.org/10.1002/ajpa.22546 CrossRefPubMedGoogle Scholar
  164. Veitschegger K (2017) The effect of body size evolution and ecology on encephalization in cave bears and extant relatives. BMC Evol Biol 17:124.  https://doi.org/10.1186/s12862-017-0976-1 CrossRefPubMedPubMedCentralGoogle Scholar
  165. Wauters LA, Lens L (1995) Effects of food availability and density on red squirrel (Sciurus vulgaris) reproduction. Ecology 76:2460–2469.  https://doi.org/10.2307/2265820 CrossRefGoogle Scholar
  166. Weisbecker V, Blomberg S, Goldizen AW, Brown M, Fisher D (2015) The evolution of relative brain size in marsupials is energetically constrained but not driven by behavioral complexity. Brain Behav Evol 85:125–135.  https://doi.org/10.1159/000377666 CrossRefPubMedGoogle Scholar
  167. West RJ (2014) The evolution of large brain size in birds is related to social, not genetic, monogamy. Biol J Linn Soc 111:668–678.  https://doi.org/10.1111/bij.12193 CrossRefGoogle Scholar
  168. West HE, Capellini I (2016) Male care and life history traits in mammals. Nat Commun 7:11854.  https://doi.org/10.1038/ncomms11854 CrossRefPubMedPubMedCentralGoogle Scholar
  169. Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz W (2014) EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027–2027.  https://doi.org/10.1890/13-1917.1 CrossRefGoogle Scholar
  170. Woodroffe R, Vincent A (1994) Mother’s little helpers: patterns of male care in mammals. Trends Ecol Evol 9:294–297.  https://doi.org/10.1016/0169-5347(94)90033-7 CrossRefPubMedGoogle Scholar
  171. Wooldridge FL (1969) Behavior of the Abyssinian Colobus monkey, Colobus guereza, in captivity. Master’s Thesis, University of South FloridaGoogle Scholar
  172. Woxvold IA, Mulder RA, Magrath MJ (2006) Contributions to care vary with age, sex, breeding status and group size in the cooperatively breeding apostlebird. Anim Behav 72:63–73.  https://doi.org/10.1016/j.anbehav.2005.08.016 CrossRefGoogle Scholar
  173. Young AJ, Carlson AA, Clutton-Brock T (2005) Trade-offs between extraterritorial prospecting and helping in a cooperative mammal. Anim Behav 70:829–837.  https://doi.org/10.1016/j.anbehav.2005.01.019 CrossRefGoogle Scholar
  174. Yu X, Zhong MJ, Li DY, Jin L, Liao WB, Kotrschal A (2018) Large-brained frogs mature later and live longer. Evolution 72:1174–1183.  https://doi.org/10.1111/evo.13478 CrossRefPubMedGoogle Scholar
  175. Zenuto RR, Antinuchi CD, Busch C (2002) Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum). Physiol Biochem Zool 75:469–478.  https://doi.org/10.1086/344739 CrossRefPubMedGoogle Scholar
  176. Zöttl M, Chapuis L, Freiburghaus M, Taborsky M (2013) Strategic reduction of help before dispersal in a cooperative breeder. Biol Lett 9:20120878.  https://doi.org/10.1098/rsbl.2012.0878 CrossRefPubMedPubMedCentralGoogle Scholar
  177. Zöttl M, Vullioud P, Goddard K, Torrents-Ticó M, Gaynor D, Bennett NC, Clutton-Brock T (2018) Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels. Physiol Behav 193:149–153.  https://doi.org/10.1016/j.physbeh.2018.03.021 CrossRefPubMedGoogle Scholar
  178. Zucker EL, Kaplan J (1981) Allomaternal behavior in a group of free-ranging patas monkeys. Am J Primatol 1:57–64.  https://doi.org/10.1002/ajp.1350010107 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of ZurichZurichSwitzerland
  2. 2.Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse FacultyUniversity of ZurichZurichSwitzerland

Personalised recommendations