Paternal care

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For paternal care in humans, see Father.

In biology, paternal care is parental investment provided by a male to his own offspring.

Parental care, by males or females, is presumed to increase growth rates, quality, and/or survival of young, and hence ultimately increase the inclusive fitness of parents.[1][2][3] In a variety of vertebrate species (e.g., ~80 of birds[4] and ~6% of mammals,[5] both males and females invest heavily in their offspring. Many of these biparental species are socially monogamous, so individuals remain with their mate for at least one breeding season.

Exclusive paternal care has evolved multiple times in a variety of organisms, including invertebrates, fishes, and amphibians.[6][7][8]

Mammals in general

Female mammals invest heavily in reproduction, in large part due to lactation. Because these costs are obvious, the physiological costs of female reproductive effort (defined as that proportion of the total energy budget of an organism that is devoted to reproductive processes[9]), especially care of offspring, have been studied extensively in mammals. These costs have been found to include reductions in longevity and in such processes as thermogenesis, physical activity, and immune function, apparently reflecting the high energetic and nutritional demands of parenting.[10][11]

Male mammals may also invest heavily in reproduction through efforts to enhance reproductive success (e.g., courtship displays, intrasexual combat) or to provide paternal care. However, the costs of paternal care have rarely been studied in mammals, in large part because only 5-10% of mammals exhibit such care.[12][13] Nonetheless, in those species in which males do provide extensive care for their offspring (i.e., biparental species, including humans), indirect evidence suggests that its costs can be substantial. For example, mammalian fathers that care for their young may undergo systematic changes in body mass and in circulating or excreted concentrations of a number of hormones (e.g., androgens, glucocorticoids, leptin) as a function of reproductive status,[14][15][16] and several of these hormones have important effects on body composition, metabolism, and organismal performance.[17][18] Nonetheless, the energetic and performance consequences of male parental investment have not been investigated directly in mammals.

In mammals, paternal care is found most commonly in primates, rodents, and canids.

Humans

Main article: Father

Human cultures and societies vary widely in the expression of paternal care. Some cultures recognize paternal care via celebration of Father's Day. According to CARTA , human paternal care is a derived characteristic (evolved in humans or our recent ancestors) and one of the defining characteristics of Homo sapiens. Different aspects of human paternal care (direct, indirect, fostering social or moral development) may have evolved at different points in our history, and together they form a unique suite of behaviors as compared with the Great Apes. One study of humans has found evidence suggesting a possible evolutionary trade-off between mating success and parenting involvement; specifically, fathers with smaller testes tend to be more involved in care of their children.[19]

According to the United States Census Bureau, approximately one third of children in the U.S. grow up without their biological father in their home. Numerous studies have documented negative consequences of being raised in a home that lacks a father, including increased likelihood of living in poverty, having behavioral problems, committing crimes, spending time in prison, abusing drugs or alcohol, becoming obese, and dropping out of school.[20]

Non-human primates

Paternal care is rare in non-human primates.[21]

Rodents

California mice (Peromyscus californicus) are very well known among mammalogists for their strongly monogamous breeding system. Unlike most small mammals, male California mice have intensive and sustained paternal behavior, and are not very promiscuous. Because of this unusual breeding and mating system, California mice have been studied extensively.

Several species of rodents have been studied as models of paternal care, including Prairie voles (Microtus ochrogaster), Campbell's dwarf hamster, the Mongolian gerbil, and the African striped mouse. The California mouse (Peromyscus californicus) is a monogamous rodent that exhibits extensive and essential paternal care, and hence has been studied as a model organism for this phenomenon.[22][23]

Birds

Fathers contribute to the care of offspring in as many as 90% of bird species, sometimes including incubating the eggs. Most paternal care is associated with biparental care in socially monogamous mating systems (about 81% of species), but in approximately 1% of species, fathers provide all care after eggs are laid.[24] The unusually high incidence of paternal care in birds compared to other vertebrate taxa is often assumed to stem from the extensive resource requirements for production of flight-capable offspring. By contrast, in bats (the other extant flying vertebrate lineage), care of offspring is provided by females (although males may help guard pups in some species[25]). In contrast to the large clutch sizes found in many bird species with biparental care, bats typically produce single offspring, which may be a limitation related to lack of male help. It has been suggested, though not without controversy, that paternal care is the ancestral form of parental care in birds.[26]

Squamates (lizards and snakes)

Although some maternal care and considerable sociality (especially in lizards[27] [28]) occurs in squamates, paternal care per se apparently has not been reported.

Fishes

Paternal care occurs in various species of fish. One well-known example of paternal care is in seahorses, where males brood the eggs in a pouch until they are ready to hatch.

Arthropods

Paternal care is rare in arthropods,[29] but occurs in some species, including the giant water bug[30][31] and the arachnid Iporangaia pustulosa, a harvestman.[32] Exclusive paternal care, where males provide the sole investment after egg-laying, is the rarest form, and is known in only 13 taxa: giant water bugs, sea spiders, two genera of leaf-footed bugs, two genera of assassin bugs, three genera of phlaeothripid thrips, three genera of harvestmen, and in millipedes of the family Andrognathidae.[33]

Theoretical models of the evolution of paternal care

Mathematical models related to the Prisoner's Dilemma suggest that when female reproductive costs are higher than male reproductive costs, males cooperate with females even when they do not reciprocate. In this view, paternal care is an evolutionary achievement that compensates for the higher energy demands that reproduction typically involves for mothers.[34]

Other models suggest that basic life-history differences between males and females are adequate to explain the evolutionary origins of maternal, paternal, and bi-parental care. Specifically, paternal care is more likely if male adult mortality is high, and maternal care is more likely to evolve if female adult mortality is high.[35] Basic life-history differences between the sexes can also cause evolutionary transitions among different sex-specific patterns of parental care.[36]

Consequences of paternal care for offspring survival and development

Care by fathers can have important consequences for survival and development of offspring in both humans[37] and other species.

Proximate mechanisms of paternal care

The proximate proximate mechanisms of paternal care are not well understood for any organism. In vertebrates, at the level of hormonal control, vasopressin apparently underlies the neurochemical basis of paternal care; prolactin and testosterone may also be involved. As with other behaviors that affect Darwinian fitness, reward pathways[38] in the brain may reinforce the expression of paternal care and may be involved in the formation of attachment bonds.

The mechanisms that underlie the onset of parental behaviors in female mammals have been characterized in a variety of species. In mammals, females undergo endocrine changes during gestation and lactation that "prime" mothers to respond maternally towards their offspring.[39][40]

Paternal males do not undergo these same hormonal changes and so the proximate causes of the onset of parental behaviors must differ from those in females. There is little consensus regarding the processes by which mammalian males begin to express parental behaviors.[41] In humans, evidence ties oxytocin to sensitive care-giving in both women and men, and with affectionate infant contact in women and stimulatory infant contact in men. In contrast, testosterone decreases in men who become involved fathers and testosterone may interfere with aspects of paternal care.[42]

Placentophagia (the behavior of ingesting the afterbirth after parturition) has been proposed to have physiological consequences that could facilitate a male’s responsiveness to offspring[43][44][45][46] Non-genomic (epigenetic) transmission of paternal behavior from fathers to their sons has been reported to occur in laboratory studies of the biparental California mouse.[47]

See also

References

  1. ↑ Lack, L. 1968. Ecological Adaptations for Breeding in Birds. Methuen, London.
  2. ↑ Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136-179 in Campbell, B., Ed., Sexual selection and the descent of Man 1871–1971. Aldine Pub, Chicago.
  3. ↑ Westneat, D. F., & Sherman, P. W. 1993. Parentage and the evolution of parental behavior. Behavioral Ecology 4:66-77.
  4. ↑ Cockburn, A. 2006. Prevalence of different modes of parental care in birds. Proceedings of the Royal Society B 273:1375-1383.
  5. ↑ Kleiman, D. G., & Malcolm, J. R., 1981. The evolution of male parental investment in mammals. Pages 347-387 in D. J. Gubernick and P. H. Klopfer, Eds., Parental care in mammals. Plenum Press, New York.
  6. ↑ Clutton-Brock, T. H. 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press.
  7. ↑ Reynolds, J. D., Goodwin, N. B., & Freckleton, R. P. 2002. Evolutionary transitions in parental care and live bearing in vertebrates. Phil Trans R Soc Lond B 357:269-281.
  8. ↑ Wesołowski, T. 2004. The origin of parental care in birds: a reassessment. Behavioral Ecology 15:520-523.
  9. ↑ Hirshfield, M. F. and D. W. Tinkle. 1975. Natural selection and the evolution of reproductive effort. Proceedings of the National Academy of Sciences of the United States of America 72:2227–2231.
  10. ↑ Jasienska G. 2009. Reproduction and lifespan: trade-offs, overall energy budgets, intergenerational costs, and costs neglected by research. Am J Hum Biol 21:524-432.
  11. ↑ Speakman JR. 2008. The physiological costs of reproduction in small mammals. Phil Trans R Soc B 363:375-398.
  12. ↑ Kleiman DG, Malcolm JR. 1981. The evolution of male parental investment in mammals. Pp 347-387 in Parental Care in Mammals, Gubernick DJ, Klopfer PH, eds. Plenum Press, New York.
  13. ↑ Woodroffe R, Vincent A. 1994. Mother’s little helpers: patterns of male care in mammals. Trends Ecol Evol 9:294-297.
  14. ↑ Campbell JC, Laugero KD, Van Westerhuyzen JA, Hostetler CM, Cohen JD, Bales KL. 2009. Costs of pair-bonding and paternal care in male prairie voles (Microtus ochrogaster). Physiol Behav 98:367-373.
  15. ↑ Wynne-Edwards KE, Timonin ME. 2007. Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 52:114-121.
  16. ↑ Ziegler TE, Prudom SL, Schultz-Darken NJ, Kurian AV, Snowdon CT. 2006. Pregnancy weight gain: marmoset and tamarin dads show it too. Biol Lett 2:181-183.
  17. ↑ Arnold, S. J. (1983). "Morphology, performance and fitness". American Zoologist 23: 347–361. 
  18. ↑ Careau, V. C.; T. Garland, Jr. (2012). "Performance, personality, and energetics: correlation, causation, and mechanism". Physiological and Biochemical Zoology 85 (6): 543–571. doi:10.1086/666970. PMID 23099454. 
  19. ↑ http://www.nature.com/news/better-fathers-have-smaller-testicles-1.13701
  20. ↑ http://blog.fatherhood.org/bid/190202/The-Father-Absence-Crisis-in-America-Infographic Accessed 17 December 2013
  21. ↑ Fernandez-Duque, Eduardo; Valeggia, Claudia R.; Mendoza, Sally P. (2009). "The Biology of Paternal Care in Human and Nonhuman Primates". Annual Review of Anthropology 38 (1): 115–130. doi:10.1146/annurev-anthro-091908-164334. 
  22. ↑ Trainor, B. C., Pride, M. C., Villalon Landeros, R., Knoblauch, N. W., Takahashi, E. Y., Silva, A. L. & Crean, K. K. 2011. Sex differences in social interaction behavior following social defeat stress in the monogamous California mouse. PLoS One, e17405.
  23. ↑ de Jong, T.R., Korosi, A., Harris, B.N., Perea-Rodrigues, J.P., and Saltzman, W. 2012. Individual variation in paternal responses of virgin male California Mice (Peromyscus californicus): Behavioral and physiological correlates. Physiological and Biochemical Zoology 85: 740-751.
  24. ↑ Cockburn, A., 2006. Prevalence of different modes of parental care in birds. Proceedings of the Royal Society B. 273 , 1375-1383
  25. ↑ Kunz, T.H. & W.R. Hood. 2000. Parental care and postnatal growth in the Chiroptera. pp 416-510 in Reproductive Biology of Bats; E. G. Chrichton, & P. H. Krutzsch, Eds. Academic Press
  26. ↑ Wesołowski, T., 2004. The origin of parental care in birds: a reassessment. Behavioral Ecology 15, 520–523.
  27. ↑ Fox, S. H., J. K. McCoy & T. A. Baird, editors. 2003. Lizard Social Behavior. Johns Hopkins University Press, Baltimore.
  28. ↑ Davis, A. R., A. Corl, Y. Surget-Groba & B. Sinervo. 2010. Convergent evolution of kin-based sociality in a lizard. Proceedings of the Royal Society B 278:1507–1514.
  29. ↑ Wong, J. W. Y., J. Meunier & M. Kolliker. 2013. The evolution of parental care in insects: the roles of ecology, life history and the social environment.
  30. ↑ Smith, R.L. 1997. Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). Pages 116–149 in The Evolution of Social Behavior in Insects and Arachnids (ed. by J. C. Choe and B. J. Crespi). Cambridge University Press, Cambridge, U.K.
  31. ↑ Ohba, S.-Y., Hidaka, K. & Sasaki, M. 2006. Notes on paternal care and sibling cannibalism in the giant water bug, Lethocerus deyrolli (Heteroptera: Belostomatidae). Entomological Science 9:1–5.
  32. ↑ Requena, G.S., Buzatto, B.A., Martins, E.G., & Machado, G. 2012. Paternal care decreases foraging activity and body condition, but does not impose survival costs to caring males in a Neotropical arachnid. PLoS ONE 7, e46701.
  33. ↑ Tallamy, Douglas W. (2001). "Evolution of exclusive paternal care in arthopods". Annual Review of Entomology 46 (1): 139–165. doi:10.1146/annurev.ento.46.1.139. 
  34. ↑ Salgado, M. 2013. The Evolution of Paternal Care. Pages 1-10 in A.M. Greenberg, W.G. Kennedy, and N.D. Bos (Eds.): SBP 2013, LNCS 7812. Springer-Verlag: Berlin, Heidelberg.
  35. ↑ Klug, H., M. B. Bonsall & S. H. Alonzo. 2013. The origin of parental care in relation to male and female life history. Ecology and Evolution 3:779-991. doi: 10.1002/ece3.493
  36. ↑ Klug, H., M. B. Bonsall & S. H. Alonzo. 2013. Sex differences in life history drive evolutionary transitions among maternal, paternal, and bi-parental care. Ecology and Evolution 3:792-806. doi: 10.1002/ece3.494
  37. ↑ http://www.zerotothree.org/child-development/early-development/how-men-and-children-affect.html
  38. ↑ http://learn.genetics.utah.edu/content/addiction/reward/
  39. ↑ Brunton, P., Russell, J., & Douglas, A. 2008. Adaptive responses of the maternal hypothalamic- pituitary-adrenal axis during pregnancy and lactation. Journal of Neuroendocrinology 20:764-776.
  40. ↑ Numan, M., & Insel, T. R. 2003. The Neurobiology of Parental Behavior. Springer, New York.
  41. ↑ Wynne-Edwards, K. E., & Timonin, M. E. 2007. Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Hormones and Behavior 52:114–121.
  42. ↑ Rilling, K. K. 2013. The neural and hormonal bases of human parental care. Neuropsychologia 51:)731–747.
  43. ↑ Gregg, J. K., & Wynne-Edwards, K. E. 2005. Placentophagia in naïve adults, new fathers, and new mothers in the biparental dwarf hamster, Phodopus campbelli. Developmental Psychobiology 47:179–188.
  44. ↑ Gregg, J. K., & Wynne-Edwards, K. E. 2006. In uniparental Phodopus sungorus, new mothers, and fathers present during the birth of their offspring, are the only hamsters that readily consume fresh placenta. Developmental Psychobiology 48:528–536.
  45. ↑ Lévy, F., & Keller, M. 2009. Olfactory mediation of maternal behavior in selected mammalian species. Behavioural Brain Research 200:336–345.
  46. ↑ Lévy, F., Keller, M., & Poindron, P. 2004. Olfactory regulation of maternal behavior in mammals. Hormones and Behavior 46:284–302.
  47. ↑ Gleason, E. D., & Marler, C. A. 2013. Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse. Proc R Soc B 280: 20130824. http://dx.doi.org/10.1098/rspb.2013.0824

Further reading

  • Gray, P. B., & Anderson, K. G. 2010. Fatherhood: Evolution and human paternal behavior. Cambridge, MA: Harvard University Press.
  • Gray, P. B., & Garcia, J. R. 2013. Evolution and human sexual behavior. Cambridge, MA: Harvard University Press.
  • Malinowski, B. 1938. The sexual life of savages. Boston: Beacon Press.
  • Muller, M. N., & Emery Thompson, M. 2012. Mating, parenting, and male reproductive strategies. In. J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombi, & J. B. Silk (Eds.), The evolution of primate societies (pp. 387–411). Chicago: The University of Chicago Press.
  • Salgado, M. 2013. The Evolution of Paternal Care. Pages 1–10 in A.M. Greenberg, W.G. Kennedy, and N.D. Bos (Eds.): SBP 2013, LNCS 7812. Springer-Verlag: Berlin, Heidelberg.
  • Smuts, B. B., & Gubernick, D. J. 1992. Male-infant relationships in nonhuman primates: Paternal investment or mating effort? In B. S. Hewlett (Ed.), Father-child relations: Cultural and biosocial contexts, (pp. 1–30). New York: Aldine.

External links

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