Social monogamy in mammalian species

Monogamous pairing refers to a general relationship between an adult male and an adult female for the purpose of sexual reproduction. It is particularly common in birds, but there are examples of this occurrence in reptiles, invertebrates, fish, amphibians, and mammals.[1]

Monogamy in mammals

Social monogamy in mammals is defined as a long term or sequential living arrangement between an adult male and an adult female (heterogeneous pair). It should not be confused with genetic monogamy, which refers to two individuals who only reproduce with one another.[2] Social monogamy does not describe the sexual interactions or patterns of reproduction between monogamous pairs; rather it strictly refers to the patterns of their living conditions.[2] Rather, sexual and genetic monogamy describe reproductive patterns. This arrangement consists of, but is not limited to: sharing the same territory; obtaining food resources; and raising offspring together. A unique characteristic of monogamy is that unlike in polygamous species, parents share parenting tasks.[3] Even though their tasks are shared, monogamy does not define the degree of paternal investment in the breeding of the young.[4]

Only ~3–5% of all mammalian species are socially monogamous, including some species that mate for life and ones that mate for an extended period of time.[4][5][6][7][8] Monogamy is more common among primates: about 29% of primate species are socially monogamous.[9] Lifelong monogamy is very rare; however, it is exemplified by species such as the prairie vole (Microtus ochrogaster).[3] A vast majority of monogamous mammals practice serial social monogamy where another male or female is accepted into a new partnership in the case of a partner's death.[2] In addition, there are some species that exhibit short-term monogamy which involves partnership termination while one's partner is still alive; however, it usually lasts for at least one breeding season.[2] Monogamy usually does not occur in groups where there is a high abundance of females, but rather in ones where females occupy small ranges.[6] Socially monogamous mammals live at significantly lower population densities than do solitary species.[9] Additionally, most mammals exhibit male-biased dispersal; however, most monogamous mammalian species display female-biased dispersal.[10]

Facultative monogamy

Facultative monogamy, or Type I monogamy, occurs when the male is not fully committed to one female, but he chooses to stay with her because there are no other mating opportunities available to him. In this type of monogamy, species rarely spend time with their families, and there is a lack of paternal care towards the offspring.[11] Elephant shrews (Rhynchocyon chrysopygus and Elephantulus rufescens), Agoutis (Dasyprocta punctata), Grey duikers (Sylvicapra grimmia), and Pacaranas (Dinomys branickii) are some of the most common examples of the mammalian species that display Type I monogamy. In addition, these species are characterized to occupy low areas over a large expand of land.[4]

Obligate monogamy

Obligate monogamy, or Type II monogamy, is practiced by species that live in overlapping territories, where females cannot rear their young without the help of their partners.[6] Species such as Indris (Indri indri), Night monkeys (Aotus trivirgatus), African dormice (Notomys alexis), and Hutias (Capromys melanurus) are observed as family groups who live together with a number of generations of their young.[4]

There are several factors that are associated with Type II monogamy:

  • high paternal investment when offspring mature in the family setting
  • delayed sexual maturation observed in juveniles that remain in the family group
  • juveniles contributing greatly to the rearing of their siblings when retained in the family group.[4]

Group living

One of the key factors of monogamous pairings is group living. Advantages to living in groups include, but are not limited to:

  • Susceptibility to predation: animals such as the dwarf mongoose (Helogale parvula) and Tamarin (such as Saguinus oedipus) may benefit from such group living by having alarm calls in response to an approaching predator.
  • Food acquisition: it is considerably easier for animals to hunt in a group rather than by themselves. For this reason, mammals such as dwarf mongooses (Helogale parvula), marmosets (Callithrix jacchus) and tamarins (like the Saguinus Oedipus) hunt in groups and share their food among their family members or members of the group.
  • Localization of resources: in some species, such as Eurasian beavers (Castor fiber), localization of an adequate lodge area (a pond or a stream) is more beneficial in a group setting. This group living arrangement gives beavers a better chance to find a high quality place to live by searching for it in a group rather than by one individual.[4]

These group living advantages, however, do not describe why monogamy, and not polygyny, has evolved in the species mentioned above. Some possible conditions which may account for cases of monogamous behavior in mammalian species may have to do with:

  • scarce resources available on any given territory so that two or more individuals are needed in order to defend it
  • physical environment conditions are so unfavorable that multiple individuals are needed to cope with it
  • early breeding serves as an advantage to the species and is crucial to monogamous species.[4]

Evolution of monogamy

There are several hypotheses for the evolution of mammalian monogamy that have been extensively studied. While some of these hypotheses apply to a majority of monogamous species, other apply to a very limited number of them.

Hormones and Neurotransmitters

Vasopressin is a hormone that induces a male prairie vole (Microtus ochrogaster) to mate with one female, form a pair bond, and exhibit mate-guarding behavior (i.e. increase the degree of monogamous behavior).[3] The presence of vasopressin receptor 1A (V1aR) in the ventral forebrain is associated with pair bonding, which is necessary for monogamy.[12] Genetic differences in the V1aR gene also play a role in monogamy: voles with long V1aR alleles exhibit more monogamous tendencies by preferring their mate over a stranger of the opposite sex, whereas voles with short V1aR alleles displayed a lesser degree of partner preference.[13] Vasopressin is responsible for forming attachment between male and female prairie voles.[3] Vasopressin also regulates paternal care.[12] Finally, vasopressin activity results in "postmating aggression" that allows prairie voles to protect their mate.[14]

Oxytocin is a hormone that regulates pair bond formation along with vasopressin.[15] Blocking either oxytocin or vasopressin prevents formation of the pair bond but continues to allow for social behavior.[16] Blocking both hormones resulted in no pair bond and reduced sociality.[16] Oxytocin also attenuates the negative effects of cortisol, a hormone related to stress, so that monogamy helps produce positive health effects. Male marmosets that received an oxytocin antagonist had increased HPA-axis activity in response to a stressor than when treated with a control,[17] showing the oxytocin associated with the pair bond lessens the physiological responses to stress. Also, marmosets who previously had elevated cortisol levels spent more time in close proximity to their mate than marmosets with previously normal cortisol levels.[18]

Dopamine, a neurotransmitter, produces pleasurable effects that reinforce monogamous behavior. Haloperidol, a dopamine antagonist, prevented partner preference but didn’t disrupt mating while apomorphine, a dopamine agonist, induced pair bonding without mating, showing dopamine is necessary for the formation of the pair bond in prairie voles.[19] In addition, mating induced a 33% increase in turnover of dopamine in the nucleus accumbens.[19] While this result was not statistically significant, it may indicate that mating can induce pair bond formation via the dopaminergic reward system.

Elevated testosterone levels are associated with decreased paternal behavior[20] and decreased testosterone levels are associated with decreased rates of infanticide. Experienced Marmoset fathers had decreased testosterone levels after exposure to their 2-week-old infant’s scent but not their 3-month-old infant’s or a stranger infant’s,[21] suggesting offspring-specific olfactory signals can regulate testosterone and induce paternal behavior.

Female distribution

Female distribution seems to be one of the best predictors of the evolution of monogamy in some species of mammals.[6] It is possible that monogamy evolved due to a low female availability or high female dispersion where males were unable to monopolize more than one mate over a period of time. In species such as Kirk's dik-dik (Madoqua kirkii) and elephant shrew (Elephantulus rufescens), biparental care is not very common. These species do, however, exhibit monogamous mating systems presumably due to high dispersal rates. Komers and Brotherton (1997) indicated that there is a significant correlation between mating systems and grouping patterns in these species. Furthermore, monogamous mating system and female dispersion are found to be closely related. Some of the main conclusions of the occurrence of monogamy in mammals include:[6]

  • Monogamy occurs when males are unable to monopolize more than one female
  • Monogamy should be more likely if female under-dispersion occurs
  • Female home range is larger for monogamous species
  • When females are solitary and occupy large ranges

This phenomenon is not common for all species,[22] but species such as the Japanese serow (Capricornis crispus) exhibits this behavior, for example.

Bi-parental care

It is believed that bi-parental care had an important role in the evolution of monogamy.[2][23] Because mammalian females undergo periods of gestation and lactation, they are well adapted to take care of their young for a long period of time, as opposed to their male partners who do not necessarily contribute to this rearing process.[2] Such differences in parental contribution could be a result of the male's drive to seek other females in order to increase their reproductive success, which may prevent them from spending extra time helping raise their offspring.[23] Helping a female in young rearing could potentially jeopardize a male's fitness and result in the loss of mating opportunities. There are some monogamous species that exhibit this type of care mainly to improve their offspring's survivorship;[4][23] however it does not occur in more than 5% of all mammals.[24]

Bi-parental care has been extensively studied in the California mouse (Peromyscus californicus). This species of mice is known to be strictly monogamous; mates pair for a long period of time, and the level of extra-pair paternity is considerably low.[25][26] It has been shown that in the event of female removal, it is the male that takes direct care of the offspring and acts as the primary hope for the survival of his young. Females who attempt to raise their young in cases where their mate is removed often do not succeed due to high maintenance costs that have to do with raising an offspring.[23] With the presence of males, the survival of the offspring is much more probable; thus, it is in the best interest for both parents to contribute.[24] This concept also applies to other species, including dwarf lemurs (Cheirogaleus medius), where females were also not successful at raising their offspring without paternal help. Lastly, in a study performed by Wynne-Edwards (1987), 95% of Djungarian hamsters (Phodopus campbelli) survived in the presence of both parents, but only 47% survived if the father was removed.[27] There are several key factors that may affect the extent to which males care for their young:[23]

  • Intrinsic ability to aid offspring: the male's ability to exhibit parental care.
  • Sociality: male paternal behavior shaped by permanent group living. There is a closer association between the male and his offspring in small groups that are often composed of individuals that are genetically related. Common examples include mongooses (Mungos mungos), wolves (Canis lupus), and naked mole-rats (Heterocephalus glaber).
  • High costs to polygyny: some males could evolve to care for their offspring in cases where females were too dispersed over the given territory and the male could not find consistent females to mate with. In those territories, individuals such as elephant shrews (Macroscelididae), and dasyproctids (Agouti, Dasyprocta, and Myoprocta), stay within their known territories rather than going outside of their limits in order to search for another mate, which would be more costly than staying around his adapted territory.
  • Paternity certainty: There are cases where males care for offspring that they are not genetically related to especially in groups where cooperative breeding is practiced. However, in some species, males are able to identify their own offspring, especially in threat of infanticide. In these groups, paternity certainty could be a factor deciding about biparental care.

Infanticide threat in larger mammals

Infanticide, the killing of the offspring by adult individuals, has been reported in many mammalian species[7][28] and it is considered as an adaptive strategy to enhance fitness. Infanticide as the result of male–male competition for reproduction will occur under the following conditions:

  • the male only kills unrelated infants
  • premature loss of her infant will result in the female going into oestrus sooner
  • the male's chance of siring the next offspring is high.[29] Infanticide by competing males is relatively common in mammals due to the length of gestation and lactation.[7]

Infanticide allows the male perpetrator to have multiple female partners; females could benefit from killing other female's offspring by gaining access to food resources or shelter.[28][30]

In primates, it is thought that risk of infanticide is the primary driver for the evolution of socially monogamous relationships.[31][7] Primates are unusual in that 25% of all species are socially monogamous; additionally, this trait has evolved separately in every major clade.[31][7][22] Primates also experience higher rates of infanticide than most other animals, with infanticide rates as high as 63% in some species.[31] Opie, Atkinson, Dunbar, & Shutlz (2013) found strong evidence that male infanticide preceded the evolutionary switch to social monogamy in primates rather than bi-parental care or female distribution, suggesting that infanticide is the main cause for the evolution of social monogamy in primates.[31]

The rates of infanticide are very low in other monogamous groups of larger mammals,[7] which can be explained by the fact that males care for their offspring and their mother by protecting them from predators and the threat of other males. This is consistent with the findings of Borries, Savini, & Koeng (2011) who indicated that the percentage of infant loss was significantly lower in monogamous species than in polyandrous ones.[7] However, there still needs to be more empirical evidence in order to further test this hypothesis.[22]

Evolutionary consequences

Sexual dimorphism relates to the phenotypic differences between a male and a female of the same species, often referring to the species' body size.[32] Monogamous males tend to be smaller compared to females, which results in sexual competition between the male candidates for a larger female.[33]

Comparing to monogamous species, polygynous species tend to display more sexual dimorphism, or difference in body size; it is believed that sexual dimorphism could be an evolutionary consequence to a monogamous mating system. In other words, monogamous animals do not compete as strongly, hence physical characteristics are not favored as much. Consequently, Weckerly (1998) concluded that mating systems do affect the extent of sexual dimorphism, with sexual dimorphism being reduced in long-term pair bonding.[4][33]

Monogamy and cooperative breeding

Cooperative breeding is defined as a social system where individuals take care of offspring other than their own. These individuals may include nonbreeding adults or subadults, alloparents, or simply reproductive adults who share the care amongst each other.[34] This care often includes provisioning for food or protection from predators. The association between cooperative breeding and monogamy has been connected to monogamous pairings within mammalian societies.[8][35]

Lukas and Clutton-Brock (2012) extensively discuss this association between monogamy and cooperative breeding.[8] Most females provision and care for their young; however, there are certain species such as mongooses (Herpestidae), New World monkeys (Callitrichidae), and porcupines (Hystrial) that care for their young in assistance of non-breeding helpers. This concept triggers the question as to why any individuals would take care of offspring other than their own. As described by the study, this social system could be triggered by the non-breeding helpers' benefit to maximize their fitness by assisting in the rearing of the young.

References
  1. Møller, Anders Pape (2003). "The evolution of monogamy: mating relationships, parental care and sexual selection". In Reichard, Ulrich H.; Boesch, Christophe (eds.). Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. pp. 29–41. ISBN 978-0-521-52577-0.
  2. Reichard, Ulrich H. (2003). "Monogamy: past and present". In Reichard, Ulrich H.; Boesch, Christophe (eds.). Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. pp. 29–41. ISBN 978-0-521-52577-0.
  3. Fackelmann, Kathy A. (1993). "Hormone of Monogamy: The Prairie Vole and the Biology of Mating". Science News. 144 (22): 360. doi:10.2307/3977640. JSTOR 3977640.
  4. Kleiman, Devra G. (1977). "Monogamy in Mammals". The Quarterly Review of Biology. 52 (1): 39–69. doi:10.1086/409721. PMID 857268.
  5. Munshi-South, Jason (2007). "Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew (Tupaia tana)". Behavioral Ecology and Sociobiology. 62 (2): 201–12. doi:10.1007/s00265-007-0454-7. JSTOR 25511685.
  6. Komers, Petr E.; Brotherton, Peter N. M. (1997). "Female space use is the best predictor of monogamy in mammals". Proceedings of the Royal Society B: Biological Sciences. 264 (1386): 1261–70. Bibcode:1997RSPSB.264.1261K. doi:10.1098/rspb.1997.0174. JSTOR 50898. PMC 1688588. PMID 9332011.
  7. Borries, Carola; Savini, Tommaso; Koenig, Andreas (2010). "Social monogamy and the threat of infanticide in larger mammals". Behavioral Ecology and Sociobiology. 65 (4): 685–93. doi:10.1007/s00265-010-1070-5.
  8. Lukas, Dieter; Clutton-Brock, Tim (2012). "Cooperative breeding and monogamy in mammalian societies". Proceedings of the Royal Society B: Biological Sciences. 279 (1736): 2151–6. doi:10.1098/rspb.2011.2468. PMC 3321711. PMID 22279167.
  9. Lukas, D.; Clutton-Brock, T. H. (2013-08-02). "The Evolution of Social Monogamy in Mammals". Science. 341 (6145): 526–530. Bibcode:2013Sci...341..526L. doi:10.1126/science.1238677. ISSN 0036-8075. PMID 23896459.
  10. Mabry, Karen E.; Shelley, Erin L.; Davis, Katie E.; Blumstein, Daniel T.; Vuren, Dirk H. Van (2013-03-06). "Social Mating System and Sex-Biased Dispersal in Mammals and Birds: A Phylogenetic Analysis". PLOS ONE. 8 (3): e57980. doi:10.1371/journal.pone.0057980. ISSN 1932-6203. PMC 3590276. PMID 23483957.
  11. Komers, Petr E. (1996). "Obligate monogamy without paternal care in Kirk's dikdik". Animal Behaviour. 51: 131–40. doi:10.1006/anbe.1996.0011.
  12. Lim, Miranda M.; Wang, Zuoxin; Olazábal, Daniel E.; Ren, Xianghui; Terwilliger, Ernest F.; Young, Larry J. (2004-06-17). "Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene". Nature. 429 (6993): 754–757. Bibcode:2004Natur.429..754L. doi:10.1038/nature02539. ISSN 1476-4687. PMID 15201909.
  13. Hammock, Elizabeth A. D.; Young, Larry J. (2005-06-10). "Microsatellite Instability Generates Diversity in Brain and Sociobehavioral Traits". Science. 308 (5728): 1630–1634. Bibcode:2005Sci...308.1630H. doi:10.1126/science.1111427. ISSN 0036-8075. PMID 15947188.
  14. Winslow, James T.; Hastings, Nick; Carter, C. Sue; Harbaugh, Carroll R.; Insel, Thomas R. (October 1993). "A role for central vasopressin in pair bonding in monogamous prairie voles". Nature. 365 (6446): 545–548. Bibcode:1993Natur.365..545W. doi:10.1038/365545a0. ISSN 0028-0836. PMID 8413608.
  15. Ross, Heather E.; Freeman, Sara M.; Spiegel, Lauren L.; Ren, Xianghui; Terwilliger, Ernest F.; Young, Larry J. (2009-02-04). "Variation in Oxytocin Receptor Density in the Nucleus Accumbens Has Differential Effects on Affiliative Behaviors in Monogamous and Polygamous Voles". The Journal of Neuroscience. 29 (5): 1312–1318. doi:10.1523/JNEUROSCI.5039-08.2009. ISSN 0270-6474. PMC 2768419. PMID 19193878.
  16. Cho, M. M.; DeVries, A. C.; Williams, J. R.; Carter, C. S. (October 1999). "The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster)". Behavioral Neuroscience. 113 (5): 1071–1079. doi:10.1037/0735-7044.113.5.1071. ISSN 0735-7044. PMID 10571489.
  17. Cavanaugh, Jon; Carp, Sarah B.; Rock, Chelsea M.; French, Jeffrey A. (April 2016). "Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys". Psychoneuroendocrinology. 66: 22–30. doi:10.1016/j.psyneuen.2015.12.027. ISSN 0306-4530. PMC 6007987. PMID 26771946.
  18. Smith, Adam S.; Birnie, Andrew K.; French, Jeffrey A. (October 2011). "Social isolation affects partner-directed social behavior and cortisol during pair formation in marmosets, Callithrix geoffroyi". Physiology & Behavior. 104 (5): 955–961. doi:10.1016/j.physbeh.2011.06.014. PMC 3183141. PMID 21712050.
  19. Aragona, Brandon J.; Liu, Yan; Curtis, J. Thomas; Stephan, Friedrich K.; Wang, Zuoxin (2003-04-15). "A Critical Role for Nucleus Accumbens Dopamine in Partner-Preference Formation in Male Prairie Voles". The Journal of Neuroscience. 23 (8): 3483–3490. doi:10.1523/jneurosci.23-08-03483.2003. ISSN 0270-6474.
  20. Nunes, Scott; Fite, Jeffrey E.; Patera, Kimberly J.; French, Jeffrey A. (February 2001). "Interactions among Paternal Behavior, Steroid Hormones, and Parental Experience in Male Marmosets (Callithrix kuhlii)". Hormones and Behavior. 39 (1): 70–82. doi:10.1006/hbeh.2000.1631. ISSN 0018-506X. PMID 11161885.
  21. Ziegler, Toni E.; Sosa, Megan E. (February 2016). "Hormonal stimulation and paternal experience influence responsiveness to infant distress vocalizations by adult male common marmosets, Callithrix jacchus". Hormones and Behavior. 78: 13–19. doi:10.1016/j.yhbeh.2015.10.004. ISSN 0018-506X. PMC 4718886. PMID 26497409.
  22. Brotherton, Peter N. M.; Komers, Petr E. (2003). "Mate guarding and the evolution of social monogamy in mammals". In Reichard, Ulrich H.; Boesch, Christophe (eds.). Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. pp. 42–58. ISBN 978-0-521-52577-0.
  23. Kleiman, Devra G.; Malcolm, James R. (1981). "The Evolution of Male Parental Investment in Mammals". In Gubernick, David J.; Klopfer, Peter H. (eds.). Parental Care in Mammals. pp. 347–87. ISBN 978-0-306-40533-4.
  24. Geary, David C. (2005). "Evolution of Paternal Investment". In Buss, David M. (ed.). The Handbook of Evolutionary Psychology. pp. 483–505. ISBN 978-0-471-72722-4.
  25. Ribble, David O. (1991). "The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting". Behavioral Ecology and Sociobiology. 29 (3): 161–166. doi:10.1007/BF00166397. JSTOR 4600601.
  26. Ribble, David O.; Salvioni, Marco (1990). "Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent". Behavioral Ecology and Sociobiology. 26 (1): 9–15. doi:10.1007/BF00174020. JSTOR 4600369.
  27. Wynne-Edwards, Katherine E. (1987). "Evidence for obligate monogamy in the Djungarian hamster, Phodopus campbelli: Pup survival under different parenting conditions". Behavioral Ecology and Sociobiology. 20 (6): 427–37. doi:10.1007/BF00302986. JSTOR 4600042.
  28. Agrell, Jep; Wolff, Jerry O.; Ylönen, Hannu; Ylonen, Hannu (1998). "Counter-Strategies to Infanticide in Mammals: Costs and Consequences". Oikos. 83 (3): 507–17. doi:10.2307/3546678. JSTOR 3546678.
  29. Hager, R.; Johnston, R. A. (2004). "Infanticide and control of reproduction in cooperative and communal breeders". Animal Behaviour. 67 (5): 941–949. doi:10.1016/j.anbehav.2003.09.009.
  30. Wolff, Jerry O. (1997). "Population Regulation in Mammals: An Evolutionary Perspective". Journal of Animal Ecology. 66 (1): 1–13. doi:10.2307/5959. JSTOR 5959.
  31. Opie, C.; Atkinson, Q. D.; Dunbar, R. I. M.; Shutlz, S. (2013). "Infanticide Leads to Social Monogamy in Primates". Proceedings of the National Academy of Sciences. National Academy of Sciences. 110 (33): 13328–13332. Bibcode:2013PNAS..11013328O. doi:10.1073/pnas.1307903110. PMC 3746880. PMID 23898180.
  32. Dobson, F. Stephen; Wigginton, John D. (1996). "Environmental influences on the sexual dimorphism in body size of western bobcats". Oecologia. 108 (4): 610–6. doi:10.1007/BF00329033. JSTOR 4221461. PMID 28307792.
  33. Weckerly, Floyd W. (1998). "Sexual-Size Dimorphism: Influence of Mass and Mating Systems in the Most Dimorphic Mammals". Journal of Mammalogy. 79 (1): 33–52. doi:10.2307/1382840. JSTOR 1382840.
  34. Solomon, Nancy G.; French, Jeffrey A., eds. (1997). Cooperative Breeding in Mammals. p. 1. ISBN 978-0-521-45491-9.
  35. Roberts, R.Lucille; Williams, Jessie R.; Wang, Alicia K.; Carter, C.SUE (1998). "Cooperative breeding and monogamy in prairie voles: Influence of the sire and geographical variation". Animal Behaviour. 55 (5): 1131–40. doi:10.1006/anbe.1997.0659. PMID 9632499.
This article is issued from Wikipedia. The text is licensed under Creative Commons - Attribution - Sharealike. Additional terms may apply for the media files.