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Paternal Care
[edit]Introduction
[edit]In biology, paternal care is parental investment provided by a male to his own offspring. It is a complex social behaviour in vertebrates associated with animal mating systems, life history traits, and ecology[1]. Paternal care may be provided alongside the mother (biparental care), or, more rarely, males can serve as the primary caregiver to their offspring. Exclusive paternal care has evolved multiple times in a variety of organisms, including invertebrates, fishes, amphibians, and in few non-human primate species[2][1]. In mammals however, forms of paternal care is commonly complimentary and in concert with the mother of the offspring. Although paternal care is well documented across species, the consequences and underlying evolutionary mechanisms as to why it evolved in the first place are still not well understood[3][4].
The role of males in infant care is rare and only occurs in approximately 5% in mammals[5]. This is because caring for an infant can result in missed mating opportunities and come at a high cost for male reproductive success[3]. Females are often observed as the main caregivers and heavily influence the survival of their own offspring however, the role of a male in infant care can have profound effects on offspring growth and development, as well as infant survival[4][3]. Within the order Primate, paternal care is thought to have evolved four times[5]. The type of care ranges from direct behaviours (grooming, playing, and transporting the infant) to indirect behaviours (protection from harassment and predators)[4][6].
Evolutionary Perspectives on Paternal Care in Primates
[edit]![](http://upload.wikimedia.org/wikipedia/commons/thumb/3/32/Squirrelmonkfamily1.jpg/220px-Squirrelmonkfamily1.jpg)
The Theory of Paternal Investment: Differences in infant care between sexes stems from females investing more time and energy in their offspring than males, while males compete with one another for access to females.[4] Although paternal care is rare among mammalians, males across many primate species still play a paternal role in infant care.
The rise of paternity in several primate species can be explained by 3 different hypotheses:
[edit]The Paternal Care hypothesis: Paternal care and investment will be designated to biological offspring, increasing the infant's chance of survival, and therefore increasing the male’s own fitness.[3][4] This hypothesis requires the on male to use recognition and behavioural cues to distinguish their own offspring from other infants.[7] Paternal uncertainty is high in multimale-multifemale primate groups so males must use these cues to recognize and bias care towards their own offspring. groups This allows males to provide both short and long-term investment for infants.[8] Primates living in monogamous pairs or single-male groups exhibit high paternity certainty and assist with the Paternal Care hypothesis.
The Mating Effort hypothesis: Males provide care for infants in order to increase mating opportunities with females.[4][9] This means that males are more likely to engage in affiliative behaviours with the infant in the presence of the mother as a form of male mating effort in order to enhance future reproductive success.[4] This theory is independent of genetics and evolved independent of paternity.
The Maternal Relief hypothesis: Males provide care infants to help reduce reproductive burdens of the female, ultimately resulting shorter inter-birth intervals and more successful offspring.[4] This stems from the male alleviating the female from her parental duties in order to keep her resources from becoming depleted and subsequently allowing her to produce high quality milk for the infant.[10] Similarly to the Mating Effort Hypothesis, the Maternal Relief hypothesis is Independent of genetics and does not require the male to be the biological father to take part in infant care.
Non-Human Primates
[edit]In non-human primates, paternal investment is often dependent on the type of mating system exhibited by each species. Mating systems influence paternity certainty and the likelihood that a male is providing care towards his own biological offspring. Paternal certainty is high in monogamous pair-bonded species and males are less likely to be at risk for caring for unrelated offspring and not contributing to their own fitness.[11][10] In contrast, polygamous primate societies create paternity uncertainty and males are more at risk of providing care for unrelated offspring and compromising their own fitness.[8][4]Paternal care by male non-human primates motivated by biological paternity utilize past mating history and phenotypic matching in order to recognize their own offspring.[12][7] Comparing male care efforts exhibited by the same species can provide insight on the significant relationship between paternity certainty and the amount of paternal care exhibited by a male. For example, Siamangs (Symphalangus syndactylus) utilize both polyandrous and monogamous mating systems but, it was found that monogamous males are more likely to carry infants and contribute to parental duties compared to those in promiscuous mating systems.[13] Studies in Primatology have used primate mating systems and social organization to help theorize the evolutionary significance of paternal care in Primates.
Strepsirrhines
[edit]![](http://upload.wikimedia.org/wikipedia/commons/thumb/1/12/Lenur_At_Monkey_World_%28190899369%29.jpeg/220px-Lenur_At_Monkey_World_%28190899369%29.jpeg)
Strepsirrhini is a suborder of the order Primates and includes lemurs, lorises, and bush babies. In this sub-order, males exhibit the lowest levels of paternal care for infants among primates.[10] Examples of observed male care in this group include playing, grooming, and occasionally transporting infants. Males have also been observed interacting with infants while mothers park them and temporarily leave in order to feed.[14][10] When female strepsirrhines park or nest their infants in nearby trees, males frequently use this as an opportunity to play with the unattended infants.[14] In this suborder, male care and affection is directed toward multiple infants including non-biological offspring, and young strepsirrhines can be found interacting with various males.[10] Paternal care does not influence infant growth rates or shorten inter-birth intervals of mothers as it can in haplorrhines.[14] Strepsirrhini males exhibit the lowest intensity of care towards infants in non-human primates.
Strepsirrhines are constrained by their life history traits and reproductive rates are not flexible within this group of primates. This group of primates are programmed to give birth when food is abundant resulting in strict seasonal breeding periods.[14]Shortening inter-birth intervals, which is theorized to be a possible outcome of increased male care, is not beneficial for Strepsirrhine mothers and can decrease infant survival.[14] Studies also show that paternity can be highly skewed in Strepsirrhines, with only one or few male members being the only biological father within a single group.[15] Instead of relying on a singular paternal figure, female mothers in this group rely on alloparenting from other group members. Infant parking and strict reproductive schedules are more beneficial for successful infant development in Strepsirrhines.
Haplorrhines
[edit]![](http://upload.wikimedia.org/wikipedia/commons/thumb/a/a5/Chimpanzee_VIII_%2813945323981%29.jpg/220px-Chimpanzee_VIII_%2813945323981%29.jpg)
Haplorhini, a sub-order of the order Primate, includes tarsiers, New World Monkeys, Old World monkeys, apes, and humans.[16] Haplorrhini is broken into two sister groups which are commonly distinguished by the characteristic of the primate nose: Catarrhini (narrow turned down nose) and Platyrrhini (flat nose). Paternal care is highly variable between the two sister groups and the species within them.[16]
Catarrhini
[edit]Catarrhini is composed of Old World Monkeys (Cercopithecidae) and Apes (Hylobatidae and Hominoidea).[17] These primates are geographically located in Africa, Asia, and Madagascar.
Cercopithecines, the largest primate family, include primates species such as baboons, macaques, colobus, and vervet monkeys.[18]
Apes consist of species of gibbons, siamangs, chimpanzees, gorillas, orangutans, and humans.[19]
Catarrhines (non-human) are often organized into a multimale-multifemale social systems and utilize polygamous mating systems which results in paternity uncertainty. It is predicted that males in promiscuous mating systems do not engage in infant care due to the high costs of caring for an infant and missing opportunities to mate with receptive females.[4] Male care in this group of primates is often portrayed through actions such as grooming, carrying, tolerance of the infant, as well as protection against agonistic interactions and infanticide.[3][4] High ranking males can also provide access to food for developing infants.[20] Direct care such as grooming and playing is not as common compared to male intervention on behalf of the infant when it is being harassed by conspecifics.[4]
![](http://upload.wikimedia.org/wikipedia/commons/thumb/f/fd/Olive_baboon_%28Papio_anubis%29_with_juvenile.jpg/220px-Olive_baboon_%28Papio_anubis%29_with_juvenile.jpg)
In Cercopiths, male involvement in the infant’s interactions with others is common in many species of baboons but between species paternal care is not always biased towards biological offspring. Male Savannah baboons (Papio cynocephalus) direct care towards their own biological offspring.[21][3] Males in this species are more likely to intervene and protect infants from harassment against other group members when the infant is predicted to be their own. Studies have shown that male Savannah baboons selectively choose to remain in closer proximity to their own offspring and engage in long-term investment beyond early infancy, when the infant is at greatest risk for infanticide.[22][3] Infants receiving paternal investment in Savannah baboons have shown enhanced fitness and accelerated maturation through males creating a safe zone for infants to exist in.[21] [22] Similarly to Savannah Baboons, Yellow baboon (Papio cynocephalus) males provide elevated care for their own offspring. Long-term care and investment beyond early infancy is better linked to paternity in this species and affecting infant growth and development.[12] Male baboons also direct care towards unrelated offspring based on male affiliations with female mothers. Baboon males and females within a social group often exhibit “friendships” with females which begin during birth of her infant and has been observed to end abruptly if the infant dies.[23][8][3] Males establish associations with females in which they have previously mated resulting in affiliative behaviour and protection towards her offspring. Relationships created by male and female members are significant for infant survival in Chacma baboons (Papio ursinus) because the risk of infanticide in early infancy is higher in this species.[23][8] Paternal care in the form of protection for the infant is therefore more beneficial than long term investment in Chacma baboons and is believed to be directed towards both biological and non-biological infants in the group.
![](http://upload.wikimedia.org/wikipedia/commons/thumb/5/5d/20171128_-_Macaca_fascicularis_-_Angkor_Wat_-_5758_DxO.jpg/220px-20171128_-_Macaca_fascicularis_-_Angkor_Wat_-_5758_DxO.jpg)
Similarly to baboons, paternal roles and the underlying mechanisms as to why paternal care evolved vary within macaque species. In Sulawesi crested macaques (Macaca nigra) both male rank and the relationship to the mother predicted male care towards an infant instead of true biological paternity[4]. In both Sulawesi and Barbary macaques (Macaca sylvanus) males adopted a “care-then-mate” strategy, in which care is provided to infants regardless of paternity in order for the male to increase future mating opportunities with the mother.[12][4] In both species, it was observed that male macaques are more likely to initiate care towards and positively interact with the infant in the presence of the mother.[4] In Assamese macaques (Macaca assamensis) biological paternity was the most significant predictor of male affiliations with infants and therefore males biased care towards infants presumed to be their own.[9][4] Observers found that Assamese males were more likely to engage and provide care for infants in the absence of their mothers reducing the likelihood that care provided to infants will impress the mother and secure access to mating possibilities.[9] In Rhesus macaques, male's providing protection and greater access to food resulted in higher weight gain for both male and female infants.[20] This had a positive effect on infant survival and was significant in the first year of infancy when the risk of infanticide is the highest.[4][20]
Chimpanzees (Pan troglodytes) are organized into fission-fusion social groups and provide an example of a polygamous mating society. Male chimpanzees often engage with infants in the form of grooming, playing, and providing protection towards other group members. In both Western and Eastern chimpanzees it was found that males were more likely to engage with their own biological offspring meaning that male care is directed by paternity in this species.[12][7] In both chimpanzee and bonobo social groups, high ranking alpha males sire approximately half of the offspring within their social group[24][25]. More research needs to be done addressing how reproductive skew affects paternal care and infant-male relationships in non-human primates including chimpanzees and bonobos.
Platyrrhines
[edit]![](http://upload.wikimedia.org/wikipedia/commons/thumb/b/b5/Goeldi%27s_marmoset%2C_Smithsonian_National_Zoo.jpg/220px-Goeldi%27s_marmoset%2C_Smithsonian_National_Zoo.jpg)
Platyrrhini is a sub-order of the order Primate and are commonly referred to as the New World Monkeys. [5] These primates occupy Central and South America, and Mexico. This group is broken into five families, range in body size, and include species such as spider monkeys, capuchins, and howler monkeys.
Among primate species, the highest levels of male care found in New World monkeys are observed in Owl monkeys (Aotus azarai ) and Titi monkeys (Callicebus caligatus). In both of these species, males and females are monogamous, pair-bonded, and exhibit bi-parental care for their offspring.[10][2][11]The social group in both these species consists of female and male parents along with their offspring.[26][11] Males in these species serve as the primary caregivers and play a major role in infant survival.[11] In both of these species, males and females are monogamous and pair-bonded. The social group in both these species consists of female and male parents along with their offspring.[26][11]
Male Titi monkeys are more involved than the mother in all aspects of male care except nursing, and engage in more social activities such as grooming, food sharing, play, and transportation of the infant.[2][11] The bond between an infant and it’s father is established right after birth and maintained into adolescence making the father the predominant attachment figure. Similarly, male Owl monkeys act as the main caregiver and are crucial to the survival of his offspring. If a female gives birth to twins, the male is still responsible for transporting both the infants.[11] In the absence of a fathers, infant mortality increases in both these species and it is unlikely that the infant will survive. One study found that the replacement of a male enacting as the role of the father also results in higher mortality during infancy emphasizing the importance of the social bond created between father and offspring at birth.[10]
![](http://upload.wikimedia.org/wikipedia/commons/thumb/4/44/Capuchin_monkey_%2813434730224%29.jpg/220px-Capuchin_monkey_%2813434730224%29.jpg)
In White‐faced Capuchins (Cebus capucinus) one study found that paternal care exhibited in the form of playful behaviour, proximity to, inspection of, and collecting discarded food items from infants was determined by male rank and dominance status rather than biological relatedness to the infant.[6] Scientists believe that future research on kin recognition needs to be done on capuchins to determine if males choose to bias their care as well as in other non-human primates.[12][6]
References
[edit]- ^ a b Stockley Paula; Hobson Liane (2016-04-27). "Paternal care and litter size coevolution in mammals". Proceedings of the Royal Society B: Biological Sciences. 283 (1829): 20160140. doi:10.1098/rspb.2016.0140. PMC 4855383. PMID 27097924.
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: CS1 maint: PMC format (link) - ^ a b c Spence-Aizenberg, Andrea; Di Fiore, Anthony; Fernandez-Duque, Eduardo (2016-1). "Social monogamy, male–female relationships, and biparental care in wild titi monkeys (Callicebus discolor)". Primates. 57 (1): 103–112. doi:10.1007/s10329-015-0489-8. ISSN 0032-8332.
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(help) - ^ a b c d e f g h Buchan, Jason C.; Alberts, Susan C.; Silk, Joan B.; Altmann, Jeanne (2003-09). "True paternal care in a multi-male primate society". Nature. 425 (6954): 179–181. doi:10.1038/nature01866. ISSN 0028-0836.
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(help) - ^ a b c d e f g h i j k l m n o p q Minge, Christin; Berghänel, Andreas; Schülke, Oliver; Ostner, Julia (2016-6). "Patterns and Consequences of Male–Infant Relationships in Wild Assamese Macaques (Macaca assamensis)". International Journal of Primatology. 37 (3): 350–370. doi:10.1007/s10764-016-9904-2. ISSN 0164-0291. PMC 4978776. PMID 27546937.
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(help)CS1 maint: PMC format (link) - ^ a b c Vargas-Pinilla, Pedro; Babb, Paul; Nunes, Leandro; Paré, Pâmela; Rosa, Gabrielle; Felkl, Aline; Longo, Dânae; Salzano, Francisco M.; Paixão-Côrtes, Vanessa R. (2017-1). "Progesterone Response Element Variation in the OXTR Promoter Region and Paternal Care in New World Monkeys". Behavior Genetics. 47 (1): 77–87. doi:10.1007/s10519-016-9806-2. ISSN 0001-8244.
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(help) - ^ a b c Sargeant, Elizabeth J.; Wikberg, Eva C.; Kawamura, Shoji; Jack, Katharine M.; Fedigan, Linda M. (2016-6). "Paternal kin recognition and infant care in white-faced capuchins ( Cebus capucinus ): Paternal Kin Recognition and Infant Care in Cebus capucinus". American Journal of Primatology. 78 (6): 659–668. doi:10.1002/ajp.22530.
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(help) - ^ a b c Fickenscher, Gisela; Lehmann, Julia; Boesch, Christophe (2006-01-01). "Kin biased investment in wild chimpanzees". Behaviour. 143 (8): 931–955. doi:10.1163/156853906778623635. ISSN 0005-7959.
- ^ a b c d Moscovice, Liza R.; Heesen, Marlies; Di Fiore, Anthony; Seyfarth, Robert M.; Cheney, Dorothy L. (2009-8). "Paternity alone does not predict long-term investment in juveniles by male baboons". Behavioral Ecology and Sociobiology. 63 (10): 1471–1482. doi:10.1007/s00265-009-0781-y. ISSN 0340-5443. PMC 2755737. PMID 19816527.
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(help)CS1 maint: PMC format (link) - ^ a b c Kerhoas, Daphne; Kulik, Lars; Perwitasari-Farajallah, Dyah; Agil, Muhammad; Engelhardt, Antje; Widdig, Anja (2016-8). "Mother-male bond, but not paternity, influences male-infant affiliation in wild crested macaques". Behavioral Ecology and Sociobiology. 70 (8): 1117–1130. doi:10.1007/s00265-016-2116-0. ISSN 0340-5443. PMC 4954837. PMID 27478299.
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(help)CS1 maint: PMC format (link) - ^ a b c d e f g Huck, Maren; Fernandez-Duque, Eduardo (2012-07-24), "When Dads Help: Male Behavioral Care During Primate Infant Development", Building Babies, Springer New York, pp. 361–385, ISBN 9781461440598, retrieved 2019-04-10
- ^ a b c d e f g Fernandez-Duque, Eduardo; Juárez, Cecilia Paola; Di Fiore, Anthony (2008-1). "Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (Aotus azarai)". Primates. 49 (1): 81–84. doi:10.1007/s10329-007-0056-z. ISSN 0032-8332.
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(help) - ^ a b c d e Murray Carson M.; Stanton Margaret A.; Lonsdorf Elizabeth V.; Wroblewski Emily E.; Pusey Anne E. "Chimpanzee fathers bias their behaviour towards their offspring". Royal Society Open Science. 3 (11): 160441. doi:10.1098/rsos.160441. PMC 5180124. PMID 28018626.
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: CS1 maint: PMC format (link) - ^ Lappan, Susan (2008-4). "Male care of infants in a siamang (Symphalangus syndactylus) population including socially monogamous and polyandrous groups". Behavioral Ecology and Sociobiology. 62 (8): 1307–1317. doi:10.1007/s00265-008-0559-7. ISSN 0340-5443.
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(help) - ^ a b c d e Tecot, S. R.; Baden, A. L.; Romine, N. K.; Kamilar, J. M. (2012-10). "Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories". Behavioral Ecology and Sociobiology. 66 (10): 1375–1386. doi:10.1007/s00265-012-1393-5. ISSN 0340-5443.
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(help) - ^ Jacobs, Rachel L.; Frankel, David C.; Rice, Riley J.; Kiefer, Vera J.; Bradley, Brenda J. (2018-2). "Parentage complexity in socially monogamous lemurs ( Eulemur rubriventer ): Integrating genetic and observational data". American Journal of Primatology. 80 (2): e22738. doi:10.1002/ajp.22738.
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(help) - ^ a b "Haplorhini", Wikipedia, 2019-03-26, retrieved 2019-04-12
- ^ "Catarrhini", Wikipedia, 2019-03-28, retrieved 2019-04-10
- ^ "Cercopithecinae", Wikipedia, 2019-01-24, retrieved 2019-04-10
- ^ "Ape", Wikipedia, 2019-04-09, retrieved 2019-04-12
- ^ a b c Widdig, Anja; Ruiz-Lambides, Angelina; Kulik, Lars; Langos, Doreen (2015-09-14). "Does Male Care, Provided to Immature Individuals, Influence Immature Fitness in Rhesus Macaques?". PLOS ONE. 10 (9): e0137841. doi:10.1371/journal.pone.0137841. ISSN 1932-6203. PMC 4569174. PMID 26367536.
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: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link) - ^ a b Patrick Ogola Onyango, Laurence R. Gesquiere, Jeanne Altmann, Susan C. Alberts. Testosterone positively associated with both male mating effort and paternal behavior in savanna baboons (Papio cynocephalus). Hormones and Behavior. Volume 63, Issue 3 2013
- ^ a b Langos, Doreen; Kulik, Lars; Mundry, Roger; Widdig, Anja (2013-7). "The impact of paternity on male-infant association in a primate with low paternity certainty". Molecular Ecology. 22 (13): 3638–3651. doi:10.1111/mec.12328. PMC 3800749. PMID 23682587.
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(help)CS1 maint: PMC format (link) - ^ a b Julia Ostner, Linda Vigilant, Jyotsna Bhagavatula, Mathias Franz, Oliver Schülke. Stable heterosexual associations in a promiscuous primate. Animal Behaviour. Volume 86 Issue 3. 2013. Pages 623-631,
- ^ Inoue, Eiji; Inoue‐Murayama, Miho; Vigilant, Linda; Takenaka, Osamu; Nishida, Toshisada (2008). "Relatedness in wild chimpanzees: Influence of paternity, male philopatry, and demographic factors". American Journal of Physical Anthropology. 137 (3): 256–262. doi:10.1002/ajpa.20865. ISSN 1096-8644.
- ^ Ishizuka Shintaro; Kawamoto Yoshi; Sakamaki Tetsuya; Tokuyama Nahoko; Toda Kazuya; Okamura Hiroki; Furuichi Takeshi. "Paternity and kin structure among neighbouring groups in wild bonobos at Wamba". Royal Society Open Science. 5 (1): 171006. doi:10.1098/rsos.171006. PMC 5792889. PMID 29410812.
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: CS1 maint: PMC format (link) - ^ a b DeLuycker, Anneke M. (2014-1). "Observations of a daytime birthing event in wild titi monkeys (Callicebus oenanthe): implications of the male parental role". Primates. 55 (1): 59–67. doi:10.1007/s10329-013-0368-0. ISSN 0032-8332.
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