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  • Cited by 11
  • Print publication year: 2010
  • Online publication date: June 2012

11 - Pair bonds and parental behaviour



Pair bonds and parental behaviour are among the most variable social traits. To understand how and why these traits are so variable, we investigate three issues in this chapter. First, we present an overview of recent work on molecular and neural aspects of pair bonds and parental care using microtine rodents as model organisms. We focus on two neuropeptides, oxytocin and vasopressin, and show that although both molecules are found in both sexes, oxytocin plays a more prominent role in regulating parenting and pair bonding in females, whereas vasopressin serves this role in males. Variation in the expression of oxytocin and vasopressin receptors appears to contribute to species and individual differences in social behaviour. These studies also show that although oxytocin and vasopressin function in distinct brain regions, they act within the same neural circuit. Therefore, females and males appear to accomplish behavioural changes in pair bonding and parental care by altering the responsiveness of the same neural circuit. Second, studies of pair bonds and parental care in natural populations have revealed that these traits are often tied together. Cost–benefit analyses of both traits in a game-theoretic framework provide novel insights into how diverse pair bonding and parental care may have evolved. Recent work emphasises the role of social environment in influencing pair bonding and care. Finally, we point out that currently there is a schism between proximate and ultimate approaches to understanding pair bonding and parental care.

Suggested readings
Balshine-Earn, S., Kempenaers, B. & Székely, T. (2002) Conflict and co-operation in parental care. Philosophical Transactions of the Royal Society B, 357, 237–404.
Hammock, E. A. D. & Young, L. J. (2005) Microsatellite instability generates diversity in brain and sociobehavioural traits. Science, 308, 1630–1634.
Houston, A. I., Székely, T. & McNamara, J. M. (2005) Conflict over parental care. Trends in Ecology and Evolution, 20, 33–38.
Reichard, U. H. (2007) Monogamy: past and present. In: Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals, ed. Reichard, U. H. & Boesch, C.Cambridge: Cambridge University Press, pp. 3–26.
Young, L. J. & Insel, T. R. (2002) Hormones and parental behaviour. In: Behavioural Endocrinology, 2nd edn, ed. Becker, J. B., Breedlove, S. M., Crews, D. & McCarthy, M. M.. Cambridge, MA: MIT Press, pp. 331–369.
Adkins-Regan, E. (2005) Hormones and Animal Social Behavior. Princeton, NJ: Princeton University Press.
Albers, H. E. & Bamshad, M. (1998) Role of vasopressin and oxytocin in the control of social behavior in Syrian hamsters (Mesocricetus auratus). Progress in Brain Research, 119, 395–408.
Alonzo, S. & Warner, R. (2000) Dynamic games and field experiments examining intra- and inter-sexual conflict: explaining counter-intuitive mating behavior in a Mediterranean wrasse, Symphodus ocellatus. Behavioral Ecology, 11, 56–70.
Aragona, B. J., Liu, Y., Yu, Y. al. (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neuroscience, 9, 133–139.
Arnqvist, G. & Rowe, L. (2005) Sexual Conflict. Princeton, NJ: Princeton University Press.
Balshine-Earn, S., Kempenaers, B. & Székely, T. (2002) Conflict and co-operation in parental care. Philosophical Transactions of the Royal Society, 357, 237–404.
Bamshad, M., Novak, M. A. & Devries, G. J. (1993) Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, M. pennsylvanicus. Journal of Neuroendocrinology, 5, 247–255.
Bateman, A. J. (1948) Intra-sexual selection in Drosophila. Heredity, 2, 349–368.
Bennett, P. M. & Owens, I. P. F. (2002) Evolutionary Ecology of Birds. Oxford:Oxford University Press.
Bester-Meredith, J. K., Young, L. J. & Marler, C. A. (1999) Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Hormones and Behavior, 36, 25–38.
Bickford, D. (2002) Male parenting of New Guinea froglets. Nature, 418, 601–602.
Bielsky, I. F. & Young, L. J. (2004) Oxytocin, vasopressin and social recognition in mammals. Peptides, 25, 1564–1574.
Bielsky, I. F., Hu, S.-B., Szegda, K. L., Westphal, H. & Young, L. J. (2004) Profound impairment in social recognition and reduction in anxiety in vasopressin V1a receptor knockout mice. Neuropsychopharmacology, 29, 483–493.
Black, J. M., ed. (1996) Partnerships in Birds. Oxford: Oxford University Press.
Bonneaud, C., Mazuc, J., Gonzalez, al. (2003) Assessing the cost of mounting an immune response. American Naturalist, 161, 367–379.
Bosch, O. J., Nair, H. P., Ahern, T., Neumann, I. D. & Young, L. J. (2009) The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology, 34, 1406–1415.
Burbach, P., Young, L. J. & Russell, J. (2006) Oxytocin: synthesis, secretion and reproductive functions. In: Knobil and Neill's Physiology of Reproduction, 3rd edn, ed. Neill, J. D.. St Louis, MO: Elsevier, pp. 3055–3128.
Cantoni, D. & Brown, R. (1997) Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Animal Behaviour, 54, 377–386.
Carter, C. S., Devries, A. C. & Getz, L. L. (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neuroscience and Biobehavioral Reviews, 19, 303–14.
Cheney, K. & Cote, I. (2003) Indirect consequences of parental care: sex differences in ectoparasite burden and cleaner-seeking activity in longfin damselfish. Marine Ecology Progress Series, 262, 267–275.
Chivian, E. & Bernstein, A. (2008) Sustaining Life. Oxford: Oxford University Press.
Clutton-Brock, T. H. (1989) Mammalian mating systems. Proceedings of the Royal Society B, 236, 339–372.
Clutton-Brock, T. H. (1991) The Evolution of Parental Care. Princeton, NJ: Princeton University Press.
Cochran, G. & Solomon, N. (2000) Effects of food supplementation on the social organization of prairie voles (Microtus ochrogaster). Journal of Mammology, 81, 746–757.
Crump, M. (1996) Parental care among the amphibia. Advances in the Study of Behavior, 25, 109–144.
Curley, J. P. & Keverne, E. B. (2005) Genes, brains and mammalian social bonds. Trends in Ecology and Evolution, 20, 561–567.
Cushing, B. S., Martin, J., Young, L. J. & Carter, C. S. (2001) The effects of peptides on partner preference formation are predicted by habitat in prairie voles. Hormones and Behavior, 39, 48–58.
Davies, N. B. (1989) Sexual conflict and the polygamy threshold. Animal Behavior, 38, 226–234.
Davies, N. B. (1991) Mating systems. In: Behavioural Ecology, 3rd edn, ed. Krebs, J. R. & Davies, N. B.. Oxford: Blackwell, pp. 263–294.
Davies, N. B. (1992) Dunnock Behaviour and Social Evolution. Oxford: Oxford University Press.
Davies, N. B. & Lundberg, A. (1984) Food distribution and a variable mating system in the dunnock (Prunella modularis). Journal of Animal Ecology, 53, 895–912.
Diesel, R., Baurle, G. & Vogel, P. (1995) Cave breeding and froglet transport: a novel pattern of anuran brood care in the Jamaican frog, Eleutherodactylus cundalli. Copeia, 1995, 354–360.
Dietz, J. (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Animal Behaviour, 46, 1067–1078.
Dunbar, R. & Dunbar, E. (1980) The pairbond in klipspringer. Animal Behaviour, 28, 219–229.
Emlen, S. T. & Oring, L. W. (1977) Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223.
Ens, B., Choudhury, S. & Black, J. M. (1996) Mate fidelity in monogamous birds. In: Partnerships in Birds, ed. J. M. Black. Oxford: Oxford University Press, pp. 344–401.
Everts, H. G. & Koolhaas, J. M. (1999) Differential modulation of lateral septal vasopressin receptor blockade in spatial learning, social recognition, and anxiety-related behaviors in rats. Behavioural Brain Research, 99, 7–16.
Ferguson, J. N., Young, L. J., Hearn, E. F., Insel., T. R. & Winslow, J. T. (2000) Social amnesia in mice lacking the oxytocin gene. Nature Genetics, 25, 284–288.
Fink, S., Excoffier, L. & Heckel, G. (2006) Mammalian monogamy is not controlled by a single gene. Proceedings of the National Academy of Sciences of the USA, 103, 10956–10960.
Forsgren, E., Amundsen, T., Borg, A. & Bjelvenmark, J. (2004) Unusually dynamic sex roles in a fish. Nature, 429, 551–554.
Fuentes, A. (1999) Reevaluating primate monogamy. American Anthropologist, 100, 890–907.
Getz, L. L. & Carter, C. S. (1996) Prairie-vole partnerships. American Scientist, 84, 56–62.
Getz, L. L. & Hofmann, J. E. (1986) Social-organization in free-living prairie voles, Microtus ochrogaster. Behavioral Ecology and Sociobiology, 18, 275–282.
Getz, L. L., Carter, C. S. & Gavish, L. (1981) The mating system of the prairie vole Microtus ochrogaster: field and laboratory evidence for pair bonding. Behavioral Ecology and Sociobiology, 8, 189–194.
Getz, L. L., Hofmann, J. E., Klatt, B., Verner, L., Cole, F. & Lindroth, R. (1987) Fourteen years of population fluctuations of Microtus ochrogaster and M. pennsylvanicus in east-central Illinois. Canadian Journal of Zoology, 65, 1317–1325.
Getz, L. L., McGuire, B., Hofmann, J. E., Pizzuto, T. & Frase, B. (1990) Social organization and mating system of the prairie vole, Microtus ochrogaster. In: Social Systems and Population Cycles in Voles, ed. Tamarin, T., Ostfeld, R., Pugh, S. & Bujalska, G.. Basel: Birkhauser, pp. 69–80.
Getz, L. L., Gudermuth, D. & Benson, S. (1992) Pattern of nest occupancy of the prairie vole, Microtus ochrogaster, in different habitats. American Midland Naturalist, 128, 197–202.
Getz, L. L., McGuire, B., Hofmann, J. E., Pizzuto, T. & Frase, B. (1993) Social organization of the prairie vole (Microtus ochrogaster). Journal of Mammalogy, 74, 44–58.
Getz, L. L., McGuire, B. & Carter, C. (2003) Social behavior, reproduction and demography of the prairie vole, Microtus ochrogaster. Ethology, Ecology and Evolution, 15, 105–118.
Gonzales-Voyeur, A., Fitzpatrick, J. & Kolm, N. (2008) Sexual selection determines parental care in cichlid fishes. Evolution, 62, 2015–2026.
Goodson, J. L. & Bass, A. H. (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin system in vertebrates. Brain Research Reviews, 35, 246–265.
Goodson, J. L., Saldanha, C., Hahn, T. & Soma, K. (2005) Recent advances in behavioral neuroendocrinology: insights from studies on birds. Hormones and Behavior, 48, 461–473.
Gowaty, P. (1996) Battles of the sexes and origins of monogamy. In: Partnerships in Birds, ed. Black, J. M.. Oxford: Oxford University Press, pp. 21–52.
Griggio, M., Matessi, G. & Pilastro, A. (2005) Should I stay or should I go? Female brood desertion and male counterstrategy in rock sparrows. Behavioral Ecology, 16, 435–441.
Gubernick, D. & Teferi, T. (2000) Adaptive significance of male parental care in a monogamous mammal. Proceedings of the Royal Society B, 267, 147–150.
Gunther, R. (2005) Derived reproductive modes in New Guinean anuran amphibians and description of a new species with paternal care in the genus Callulops (Microhylidae). Journal of Zoology, 268, 153–170.
Hammock, E. A. D. & Young, L. J. (2004) Functional microsatellite polymorphisms associated with divergent social structure in vole species. Molecular Biology and Evolution, 21, 1057–1063.
Hammock, E. A. D. & Young, L. J. (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science, 308, 1630–1634.
Hammock, E. A. D. & Young, L. J., eds. (2007a) Neuroendocrinology, Neurochemistry, and Molecular Neurobiology of Affiliative Behavior. New York, NY: Springer-Verlag.
Hammock, E. A. D. & Young, L. J. (2007b) On switches and knobs, microsatellites and monogamy. Trends in Genetics, 23, 209–212.
Hansell, M. (2000) Bird Nests and Construction Behaviour. Cambridge: Cambridge University Press.
Harrison, F., Barta, Z., Cuthill, I. & Székely, T. (2009) How is sexual conflict over parental care resolved: a meta-analysis. Journal of Evolutionary Biology, 22, 1800–1812.
Houston, A. I. & Davies, N. B. (1985) Evolution of cooperation and life history in dunnocks. In: Behavioural Ecology: the Ecological Consequences of Adaptive Behaviour, ed. Sibly, R. & Smith, R. H.Oxford: Blackwell, pp. 471–487.
Houston, A. I., Székely, T. & McNamara, J. (2005) Conflict over parental care. Trends in Ecology and Evolution, 20, 33–38.
Hunt, J. & Simmons, L. (2002) Behavioural dynamics of biparental care in the dung beetle Onthophagus taurus. Animal Behaviour, 64, 65–75.
Ims, R. (1987) Responses in spatial organisation and behaviour to manipulations of the food resource in the vole Clethrionomys rufocanus. Journal of Animal Ecology, 56, 585–596.
Insel, T. R. & Hulihan, T. (1995) A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behavioral Neuroscience, 109, 782–789.
Insel, T. R. & Shapiro, L. E. (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the USA, 89, 5981–5985.
Insel, T. R. & Young, L. J. (2000) Neuropeptides and the evolution of social behavior. Current Opinion in Neurobiology, 10, 784–789.
Insel, T. R., Wang, Z. & Ferris, C. F. (1994) Patterns of vasopressin receptor distribution associated with social organization in microtine rodents. Journal of Neuroscience, 14, 5381–5392.
Itzkowitz, M., Santangelo, N. & Richter, M. (2001) Parental division of labour and the shift from minimal to maximal role specializations: an examination using a biparental fish. Animal Behaviour, 61, 1237–1245.
Ivell, R. & Dietmar, R. (1985) Structure and comparison of the oxytocin and vasopressin genes from rat. Proceedings of the National Academy of Sciences of the USA, 81, 2006–2010.
Jennions, M. & Petrie, M. (2000) Why do females mate multiply? A review of the genetic benefits. Biological Reviews, 59, 677–688.
Johnstone, R. A. & Hinde, C. A. (2006) Negotiation over offspring care: how should parents respond to each other's efforts?Behavioral Ecology, 17, 818–827.
Kempenaers, B. (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Advances in the Study of Behavior, 37, 189–278.
Kendrick, K. M., Keverne, E. B. & Baldwin, B. A. (1987) Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology, 46, 56–61.
Kendrick, K. M., Costa, A. P. C. D., Broad, K. al. (1997) Neural control of maternal behavior and olfactory recognition of offspring. Brain Research Bulletin, 44, 383–395.
Kock, K. & Pshenichnov, (2006) Evidence for egg brooding and parental care in icefish and other notothenioids in the Southern Ocean. Antarctic Science, 18, 223–227.
Kokko, H. & Jennions, M. (2003) It takes two to tango. Trends in Ecology and Evolution, 18, 103–104.
Kokko, H. & Jennions, M. (2008) Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21, 919–948.
Kolm, N., Goodwin, N., Balshine, S. & Reynolds, J. (2006) Life history evolution in cichlids 1: revisiting the evolution of life histories in relation to parental care. Journal of Evolutionary Biology, 19, 66–75.
Komers, P. & Brotherton, P. (1997) Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society B, 264, 1261–1270.
Kosztolányi, A., Székely, T., Cuthill, I., Yilmaz, K. & Berberoglu, S. (2006) The influence of habitat on brood-rearing behaviour in the Kentish plover. Journal of Animal Ecology, 75, 257–265.
Kupfer, A., Muller, H., Antoniazzi, al. (2006) Parental investment by skin feeding in a caecilian amphibian. Nature, 440, 926–929.
Lack, D. (1968) Ecological Adaptations for Breeding in Birds, London: Methuen.
Landgraf, R., Gerstberger, R., Montkowski, al. (1995) V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. Journal of Neuroscience, 6, 4250–4258.
Landgraf, R., Frank, E., Aldag, J. al. (2003) Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour. European Journal of Neuroscience, 18, 403–411.
Leengoed, E. V., Kerker, E. & Swanson, H. H. (1987) Inhibition of postpartum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. Journal of Endocrinology, 112, 275–282.
Lehtinen, R. & Nussbaum, R. (2003) Parental care: a phylogenetic perspective. In: Reproductive Biology and Phylogeny of Anura, ed. Jamieson, B. G. M.. Enfield, NH: Science Publishers, pp. 343–386.
Lessells, C. M. (1999) Sexual conflict in animals. In: Levels of Selection in Evolution, ed. Keller, L.. Princeton, NJ: Princeton University Press, pp. 75–99.
Ligon, J. (1999) Evolution of Avian Breeding Systems. New York, NY: Oxford University Press.
Liker, A. (1995) Monogamy in precocial birds: a review. Ornis Hungarica, 5, 1–14.
Liker, A. & Székely, T. (1997) Aggression among female lapwings, Vanellus vanellus. Animal Behaviour, 54, 797–802.
Lim, M. M., Murphy, A. & Young, L. J. (2004a) Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster). Journal of Comparative Neurology, 468, 555–570.
Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwillger, E. F. & Young, L. J. (2004b) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature, 429, 754–757.
Liu, Y., Curtis, J. T. & Wang, Z. (2001) Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behavioral Neuroscience, 115, 910–919.
Lonstein, J. & Vries, G. (1999) Comparison of the parental behavior of pairbonded female and male prairie voles (Microtus ochrogaster). Physiology and Behavior, 66, 33–40.
Lott, D. (1991) Intraspecific Variation in the Social Systems of Wild Vertebrates. Cambridge: Cambridge University Press.
Lucia, K., Keane, B., Hayes, al. (2008) Philopatry in prairie voles: an evaluation of the habitat saturation hypothesis. Behavioral Ecology, 19, 774–783.
Mank, J. & Avise, J. (2006) The evolution of reproductive and genomic diversity in ray-finned fishes: insights from phylogeny and comparative analysis. Journal of Fish Biology, 69, 1–27.
McGuire, B. & Bemis, W. E. (2007) Parental care. In: Rodent Societies: an Ecological and Evolutionary Perspective, ed. Wolff, J. O. & Sherman, P. W.. Chicago, IL: University of Chicago Press, pp. 231–242.
McGuire, B. & Novak, M. (1984a) A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Animal Behaviour, 32, 1132–1141.
McGuire, B. & Novak, M. (1984b) A comparison of maternal behaviors in the meadow vole, prairie vole and pine vole. Animal Behaviour, 32, 1132–1141.
McKinney, F., Cheng, K. & Bruggers, D. (1984) Sperm competition in apparently monogamous birds. In: Sperm Competition and the Evolution of Animal Mating Systems, ed. Smith, R. L.. New York, NY: Academic Press, pp. 523–545.
McNamara, J. M. & Forslund, P. (1996) Divorce rates in birds: predictions from an optimization model. American Naturalist, 147, 609–640.
McNamara, J. M., Gasson, C. & Houston, A. (1999) Incorporating rules for responding into evolutionary games. Nature, 401, 368–371.
McNamara, J. M., Houston, A., Barta, Y. & Osorno, J.-L. (2002) Should young ever be better off with one parent than with two?Behavioral Ecology, 14, 301–310.
Meaney, M. J. (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience, 24, 1161–1192.
Mock, D. W. & Parker, G. A. (1997) The Evolution of Sibling Rivalry. Oxford:Oxford University Press.
Møller, A. (2007) The evolution of monogamy: mating relationships, parental care and sexual selection. In: Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals, ed. Reichard, U. H. & Boesch, C.. Cambridge: Cambridge University Press, pp. 29–41.
Nettle, D. (2008) Why do some dads get more involved than others? Evidence from a large British cohort. Evolution and Human Behavior, 29, 416–423.
Numan, M. & Insel, T. R. (2003) The Neurobiology of Parental Behavior. New York, NY: Springer-Verlag.
Ó Foighil, D. & Taylor, D. (2000) Evolution of parental care and ovulation behavior in oysters. Phylogenetics and Evolution, 15, 301–313.
Olazábal, D. E. & Young, L. J. (2005) Variability in ‘spontaneous’ maternal behavior is associated with anxiety-like behavior and affiliation in naive juvenile and adult female prairie voles (Microtus ochrogaster). Developmental Psychobiology, 47, 166–178.
Olazábal, D. E. & Young, L. J. (2006a) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Hormones and Behavior, 49, 681–687.
Olazábal, D. E. & Young, L. J. (2006b) Oxytocin receptors in the nucleus accumbens facilitate ‘spontaneous’ maternal behavior in adult female prairie voles. Neuroscience, 141, 559–568.
Oliveras, D. & Novak, M. (1986) A comparison of paternal behavior in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster. Animal Behaviour, 34, 519–526.
Ophir, A.G., Phelps, S.M., Sorin, A.B. & Wolff, J.O. (2007) Morphological, genetic, and behavioural comparisons of two prairie vole populations in the field and laboratory. Journal of Mammalogy, 88, 989–999.
Ophir, A. G., Phelps, S. M., Sorin, A. B. & Wolff, J. O. (2008a) Social but not genetic monogamy is associated with greater breeding success in prairie voles. Animal Behaviour, 75, 1143–1154.
Ophir, A. G., Campbell, P., Hanna, K. & Phelps, S. M. (2008b) Field tests of cis-regulatory variation at the prairie vole avpr1a locus: Association with V1aR abundance but not sexual or social fidelity. Hormones and Behavior, 54, 694–702.
Ophir, A., Wolff, J. & Phelps, S. (2008c) Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proceedings of the National Academy of Sciences of the USA, 105, 1249–1254.
Osorno, J. & Székely, T. (2004) Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females. Animal Behaviour, 68, 337–342.
Ostfeld, R. (1986) Territoriality and mating systems of California voles. Journal of Animal Ecology, 55, 691–706.
Pedersen, C. A. & Prange, A. J. (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proceedings of the National Academy of Sciences of the USA, 76, 6661–6665.
Pedersen, C. A., Caldwell, J., Walker, C., Ayers, G. & Mason, G. (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behavioral Neuroscience, 108, 1163–1171.
Persson, O. & Öhrström, P. (1989) A new avian mating system: ambisexual polygamy in the penduline titRemiz pendulinus. Ornis Scandinavica, 20, 105–111.
Pilastro, A., Biddau, T., Marin, G. & Mingozzi, T. (2001) Female brood desertion increases with number of available mates in the rock sparrow. Journal of Avian Biology, 32, 68–72.
Pizzuto, T. & Getz, L. L. (1998) Female prairie voles (Microtus ochrogaster) fail to form a new pair after loss of mate. Behavioural Processes, 43, 79–86.
Poelman, E. & Dicke, M. (2007) Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evolutionary Ecology, 21, 215–227.
Raadik, T., Bourke, D., Clarke, M. & Martin, A. (1990) Behaviour and reproductive success of pairs and lone parents in the convict cichlidHeros nigrofasciatus. Animal Behaviour, 39, 594–596.
Rauter, C. M. & Moore, A. J. (2004) Time constraints and trade-offs among parental care behaviours: effects of brood size, sex and loss of mate. Animal Behaviour, 68, 695–702.
Reichard, U. H. (2007) Monogamy: past and present. In: Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals, ed. Reichard, U. H. & Boesch, C.. Cambridge: Cambridge University Press, pp. 3–26.
Reynolds, J. D., Goodwin, N. B. & Freckleton, R. P. (2002) Evolutionary transitions in parental care and live-bearing in vertebrates. Philosophical Transactions of the Royal Society B, 357: 269–281.
Roberts, R. L., Miller, A. K., Taymans, S. E. & Carter, C. S. (1998) Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster). Canadian Journal of Zoology, 76, 1862–1868.
Royle, N., Hartley, I. & Parker, G. (2002) Sexual conflict reduces offspring fitness in zebra finches. Nature, 416, 733–736.
Sanz, J., Kranenbarg, S. & Tinbergen, J. (2000) Differential response by males and females to manipulation of partner contribution in the great tit (Parus major). Journal of Animal Ecology, 69, 74–84.
Searcy, W. & Yasukawa, K. (1995) Polygyny and Sexual Selection in Red-Winged Blackbirds. Princeton, NJ: Princeton University Press.
Slagsvold, T. & Lifjeld, J. T. (1994) Polygyny in birds: the role of competition between females for male parental care. American Naturalist, 143, 59–94.
Smiseth, P. T., Dawson, C., Varley, E. & Moore, A. J. (2005) How do caring parents respond to mate loss? Differential response by males and females. Animal Behaviour, 69, 551–559.
Solomon, N. G. (1991) Current indirect fitness benefits associated with philopatry in juvenile prairie voles. Behavioral Ecology and Sociobiology, 29, 277–282.
Solomon, N. G. (1993) Comparison of parental behavior in male and female prairie voles (Microtus ochrogaster). Canadian Journal of Zoology, 71, 434–437.
Solomon, N. G. & Crist, T. (2008) Estimates of reproductive success for group-living prairie voles, Microtus ochrogaster, in high-density populations. Animal Behaviour, 76, 881–892.
Solomon, N. G. & Keane, B. (2007) Reproductive strategies in female rodents. In: Rodent Societies: an Ecological and Evolutionary Perspective, ed. Wolff, J. O. & Sherman, P. W.. Chicago, IL: University of Chicago Press, pp. 42–56.
Solomon, N. G., Keane, B., Knoch, L. & Hogan, P. (2004) Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster). Canadian Journal of Zoology, 82, 1667–1671.
Soma, K. (2006) Testosterone and aggression: Berthold, birds and beyond. Journal of Neuroendocrinology, 18, 543–551.
Summers, K., Mckeon, C. & Heying, H. (2006) The evolution of parental care and egg size: a comparative analysis in frogs. Proceedings of the Royal Society B, 273, 687–692.
Székely, T., Cuthill, I. & Kis, J. (1999) Brood desertion in Kentish plover: sex differences in remating opportunities. Behavioral Ecology, 10, 983–993.
Székely, T., Webb, J. & Cuthill, I. (2000) Mating patterns, sexual selection and parental care: an integrative approach. In: Vertebrate Mating Systems, ed. Apollonio, M., Festa-Bianchet, M. & Mainardi, D.. London: World Science Press, pp. 194–223.
Szentirmai, I., Székely, T. & Komdeur, J. (2007) Sexual conflict over care: antagonistic effects of clutch desertion on reproductive success of male and female penduline tits. Journal of Evolutionary Biology, 20, 1739–1744.
Tallamy, D. (1999) Semelparity and the evolution of maternal care in insects. Animal Behavior, 57, 2373–2383.
Thomas, G. & Székely, T. (2005) Evolutionary pathways in shorebird breeding systems: sexual conflict, parental care, and chick development. Evolution, 59, 2222–2230.
Thomas, G., Freckleton, R. & Székely, T. (2006) Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds. Proceedings of the Royal Society B, 273, 1619–1624.
Tieleman, B. I., Dijkstra, T., Klasing, K., Visser, G. & Williams, J. (2008) Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrensBehavioral Ecology, 19, 949–959.
Tregenza, T. & Wedell, N. (2000) Genetic compatibility, mate choice and patterns of parentage. Molecular Ecology, 9, 1013–1027.
Trivers, R. L. (1972) Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871–1971, ed. Campbell, B.. Chicago, IL: Aldine, pp. 136–179.
Trivers, R. L. (1974) Parent–offspring conflict. American Zoologist, 14, 249–264.
Tyler, M. & Carter, D. (1981) Oral birth of the young of the gastric brooding frog Rheobatrachus silus. Animal Behaviour, 29, 280–282.
Veiga, J. (1992) Why are house sparrows predominantly monogamous: a test of hypotheses. Animal Behaviour, 43, 361–370.
Walling, C. A., Stamper, C. E., Smiseth, P. T. & Moore, A. J. (2008) Genetic architecture of sex differences in parental care. Proceedings of the National Academy of Sciences of the USA, 105, 18430–18435.
Wang, Z., Ferris, C. F. & Vries, G. J. (1994) Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proceedings of the National Academy of Sciences of the USA, 91, 400–4.
Wang, Z., Zhou, L., Hulihan, T. J. & Insel, T. R. (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. Journal of Comparative Neurology, 366, 726–737.
Wang, Z. X. & Insel, T. R. (1996) Parental behavior in voles. Advances in the Study of Behavior, 25, 361–384.
Westneat, D. F. & Stewart, I. R. K. (2003) Extra-pair paternity in birds: causes, correlates and conflict. Annual Review of Ecology, Evolution and Systematics, 34, 365–396.
Whittingham, L., Dunn, P. & Robertson, R. (1994) Female response to reduced male parental care in birds: an experiment in tree swallows. Ethology, Ecology and Evolution, 96, 260–269.
Williams, J. R., Catania, K. & Carter, C. (1992) Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Hormones and Behavior, 26, 339–349.
Williams, J. R., Insel, T. R., Harbaugh, C. R. & Carter, C. S. (1994) Oxytocin administered centrally facilitates formation of a partner preference in prairie voles (Microtus ochrogaster). Journal of Neuroendocrinology, 6, 247–250.
Williams, T. (1996) Mate fidelity in penguins. In: Partnerships in Birds, ed. Black, J. M.. Oxford: Oxford University Press, pp. 268–285.
Wilson, E. O. (1975) Sociobiology: the New Synthesis, Cambridge, MA:Harvard University Press.
Wingfield, J., Hegner, R.-E., Dufty Jr., A. & Ball, G. (1990) The ‘challenge hypothesis’: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. American Naturalist, 136, 829–846.
Winslow, J., Hastings, N., Carter, C. S., Harbaugh, C. & Insel., T. (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature, 365, 545–548.
Wise, R. A. (2002) Brain reward circuitry: insights from unsensed incentives. Neuron, 36, 229–240.
Wolff, J. O. & MacDonald, D. W. (2004) Promiscuous females protect their offspring. Trends in Ecology and Evolution, 19, 127–134.
Wright, J. & Cuthill, I. (1990) Biparental care: short-term manipulations of partner contribution and brood size in the starling. Behavioral Ecology, 1, 116–124.
Young, L. J. (1999) Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Hormones and Behavior, 36, 212–221.
Young, L. J. & Insel, T. R. (2002) Hormones and parental behaviour. In: Behavioral Endocrinology, 2nd edn, ed. Becker, J. B., Breedlove, S. M., Crews, D. & McCarthy, M. M.. Cambridge, MA: MIT Press, pp. 331–369.
Young, L. J. & Wang, Z. (2004) The neurobiology of pair bonding. Nature Neuroscience, 7, 1048–1054.
Young, L. J., Wang, Z. & Insel, T. R. (1999) Neuroendocrine bases of monogamy. Trends in Neuroscience, 21, 71–75.
Young, L. J., Lim, M. M., Gingrich, B. & Insel, T. R. (2001) Cellular mechanisms of social attachment. Hormones and Behavior, 40, 133–138.
Yu, G.-Z., Kaba, H., Okutani, F. & Higuchi, T. (1996) The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience, 72, 1083–1088.
Zeh, J. & Zeh, D. (2001) Reproductive mode and the genetic benefits of polyandry. Animal Behaviour, 61, 1051–1063.