Paternal care

Not to be confused with Parenting or Parental investment.
For paternal care in humans, see Father.

In biology, paternal care is parental investment provided by a male animal to his own offspring. Paternal care may provided in concert with the mother (biparental care) or, more rarely, by the male alone (so called exclusive paternal care).

The provision of care, by either 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., about 80% of birds[4] and about 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

Male mammals may 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.[9][10] 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,[11][12][13] and several of these hormones have important effects on body composition, metabolism, and organismal performance.[14][15] Nonetheless, the energetic and performance consequences of male parental investment have rarely been investigated directly in mammals.[16]

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.[17]

Research on the effects of paternal care on human happiness have yielded conflicting results. However, one recent study concluded that fathers generally report higher levels of happiness, positive emotion, and meaning in life as compared with non-fathers.[18]

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.[19]

Non-human primates

Paternal care is rare in non-human primates.[20]

Rodents

California mice (Peromyscus californicus) are well known for have intensive and sustained paternal behavior.

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.[21][22] One study of this species found that fathers had larger hindlimb muscles than did non-breeding males.[16]

Birds

Fathers contribute equally with mothers 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.[4] 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[23]). 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.[8]

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Amphibians

Paternal care occurs in a number of species of anuran amphibians,[24] including glass frogs.

Fish

Paternal care occurs in perhaps as many as half of the known species of certain families of teleost fish. One well-known example of paternal care is in seahorses, where males brood the eggs in a brood pouch until they are ready to hatch.

In jawfish, the female lays the eggs and the male then takes them in his mouth. A male can have up to 400 eggs in his mouth at one time. The male can't feed while he hosts the young, but as the young get older, they spend more time out of the mouth.[25]

During the breeding season, male three-spined sticklebacks defend nesting territories. Males attract females to spawn in their nests and defend their breeding territory from intruders and predators. After spawning, the female leaves the male’s territory and the male is solely responsible for the care of the eggs. During the ~6-day incubation period, the male ‘fans’ (oxygenates) the eggs, removes rotten eggs and debris, and defends the territory. Even after embryos hatch, father sticklebacks continue to tend their newly hatched offspring for ~7 days, chasing and retrieving fry that stray from the nest and spiting them back into the nest.[26]

Arthropods

Paternal care is rare in arthropods,[27] but occurs in some species, including the giant water bug[28][29] and the arachnid Iporangaia pustulosa, a harvestman.[30] In several species of crustaceans, males provide care of offspring by building and defending burrows or other nest sites.[31] 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.[32]

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.[33]

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.[34] Basic life-history differences between the sexes can also cause evolutionary transitions among different sex-specific patterns of parental care.[35]

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[36] and other species. Mechanisms underlying such effects may include protecting offspring from predators or environmental extremes (e.g., heat or cold), feeding them or, in some species, direct teaching of skills. Moreover, some studies indicate a potential epigenetic germline inheritance of paternal effects.[37]

The effects of paternal care on offspring can be studied in various ways. One way is to compare species that vary in the degree of paternal care. For example, an extended duration of paternal care occurs in the gentoo penguin, as compared with other Pygoscelis species. It was found that their fledging period, the time between a chick’s first trip to sea and its absolute independence from the group, was longer than other penguins of the same genus. The authors hypothesized that this was because it allowed chicks to better develop their foraging skills before becoming completely independent from their parents. By doing so, a chick may have a higher chance of survival and increase the population’s overall fitness.[38]

Proximate mechanisms of paternal care

The 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[39] 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.[40][41]

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.[42] 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.[43]

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[44][45][46][47] Non-genomic transmission of paternal behavior from fathers to their sons has been reported to occur in laboratory studies of the biparental California mouse, but whether this involves (epigenetic) modifications or other mechanisms is not yet known.[48]

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. doi:10.1093/beheco/4.1.66.
  4. 1 2 Cockburn, A (2006). "Prevalence of different modes of parental care in birds". Proceedings of the Royal Society B. 273: 1375–1383. doi:10.1098/rspb.2005.3458. PMC 1560291Freely accessible. PMID 16777726.
  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. doi:10.1098/rstb.2001.0930. PMC 1692951Freely accessible. PMID 11958696.
  8. 1 2 Wesołowski, T (2004). "The origin of parental care in birds: a reassessment". Behavioral Ecology. 15: 520–523. doi:10.1093/beheco/arh039.
  9. ↑ 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.
  10. ↑ Woodroffe, R; Vincent, A (1994). "Mother's little helpers: patterns of male care in mammals". Trends Ecol Evol. 9: 294–297. doi:10.1016/0169-5347(94)90033-7. PMID 21236858.
  11. ↑ 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. doi:10.1016/j.physbeh.2009.06.014.
  12. ↑ 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.
  13. ↑ 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. doi:10.1098/rsbl.2005.0426.
  14. ↑ Arnold, S. J. (1983). "Morphology, performance and fitness" (PDF). American Zoologist. 23: 347–361. doi:10.1093/icb/23.2.347.
  15. ↑ Careau, V. C.; T. Garland, Jr. (2012). "Performance, personality, and energetics: correlation, causation, and mechanism" (PDF). Physiological and Biochemical Zoology. 85 (6): 543–571. doi:10.1086/666970. PMID 23099454.
  16. 1 2 Andrew, J. R., W. Saltzman, M. A. Chappell, and T. Garland, Jr. 2016. Consequences of fatherhood in the biparental California mouse (Peromyscus californicus): locomotor performance, metabolic rate, and organ masses. Physiological and Biochemical Zoology 89:130–140.
  17. ↑ http://www.nature.com/news/better-fathers-have-smaller-testicles-1.13701
  18. ↑ Nelson, S. K.; Kushlev, K.; English, T.; Dunn, E. W.; Lyubomirsky, S. (2013). "In Defense of Parenthood: Children Are Associated With More Joy Than Misery". Psychological Science. 24: 3–10. doi:10.1177/0956797612447798.
  19. ↑ http://blog.fatherhood.org/bid/190202/The-Father-Absence-Crisis-in-America-Infographic Accessed 17 December 2013
  20. ↑ 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.
  21. ↑ 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.
  22. ↑ De Jong, T.R.; Korosi, A.; Harris, B.N.; Perea-Rodrigues, J.P.; 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. doi:10.1086/665831.
  23. ↑ 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
  24. ↑ Brown, J. L.; Morales, V.; Summers, K. (2010). "A key ecological trait drove the evolution of biparental care and monogamy in an amphibian". The American Naturalist. 175: 436–446. doi:10.1086/650727. PMID 20180700.
  25. ↑ Taylor, A-L. (2012). "Shells, trees and bottoms: Strange places fish live". BBC. Retrieved February 26, 2015.
  26. ↑ Wootton, Robert. A Functional Biology of Sticklebacks. Berkeley: University of California Press.
  27. ↑ 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.
  28. ↑ 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.
  29. ↑ 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. doi:10.1111/j.1479-8298.2006.00147.x.
  30. ↑ 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. doi:10.1371/journal.pone.0046701.
  31. ↑ Duffy, S. E. 2010. Crustacean social evolution, in: Encyclopedia of Animal Behavior. Elsevier, pp. 421–429.
  32. ↑ Tallamy, Douglas W. (2001). "Evolution of exclusive paternal care in arthropods". Annual Review of Entomology. 46 (1): 139–165. doi:10.1146/annurev.ento.46.1.139.
  33. ↑ 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.
  34. ↑ Klug, H.; Bonsall, M. B.; Alonzo, S. H. (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.
  35. ↑ Klug, H.; Bonsall, M. B.; Alonzo, S. H. (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.
  36. ↑ http://www.zerotothree.org/child-development/early-development/how-men-and-children-affect.html
  37. ↑ Curley, J. P., R. Mashoodh, and F. A. Champagne. 2011. Epigenetics and the origins of paternal effects. Hormones and Behavior 59:306–314.
  38. ↑ Polito, Michael J., and Wayne Z. Trivelpiece. "Transition to Independence and Evidence of Extended Parental Care in the Gentoo Penguin (Pygoscelis Papua)." Marine Biology (2008): n. pag. WorldCat@OSU. Web. Sept. 2014.
  39. ↑ http://learn.genetics.utah.edu/content/addiction/reward/
  40. ↑ 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. doi:10.1111/j.1365-2826.2008.01735.x.
  41. ↑ Numan, M., & Insel, T. R. 2003. The Neurobiology of Parental Behavior. Springer, New York.
  42. ↑ 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.
  43. ↑ Rilling, K. K. (2013). "The neural and hormonal bases of human parental care". Neuropsychologia. 51: 731–747. doi:10.1016/j.neuropsychologia.2012.12.017.
  44. ↑ 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. doi:10.1002/dev.20079.
  45. ↑ 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. doi:10.1002/dev.20174.
  46. ↑ Lévy, F.; Keller, M. (2009). "Olfactory mediation of maternal behavior in selected mammalian species". Behavioural Brain Research. 200: 336–345. doi:10.1016/j.bbr.2008.12.017.
  47. ↑ Lévy, F.; Keller, M.; Poindron, P. (2004). "Olfactory regulation of maternal behavior in mammals". Hormones and Behavior. 46: 284–302. doi:10.1016/j.yhbeh.2004.02.005.
  48. ↑ 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. doi:10.1098/rspb.2013.0824.

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