Social but not genetic monogamy is associated with greater breeding success in prairie voles

Ophir, Alexander G.; Phelps, Steve; Sorin, Anna Bess; Wolff, Jerry O.

doi:10.1016/j.anbehav.2007.09.022

Cited by 113 publications

(179 citation statements)

References 47 publications

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“…In natural prairie vole populations, approximately one-half of males "wander" across multiple female territories attempting to mate with multiple females Solomon and Jacquot, 2002), and the biological basis of this variation continues to be studied (Fink et al, 2006;Young and Hammock, 2007;Ophir et al, 2008;Mabry et al, 2011). It was shown previously that environmental factors also contribute to mating strategy in this species as male prairie voles do not show partner preferences after long-term cohabitation unless pregnancy is established soon after pairing (Curtis, 2010).…”

Section: Fecundity and Pair Bondingmentioning

confidence: 99%

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

et al. 2012

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The prairie vole is a socially monogamous species in which breeder pairs typically show strong and selective pair bonds. The establishment of a pair bond is associated with a behavioral transition from general affiliation to aggressive rejection of novel conspecifics. This "selective aggression" is indicative of mate guarding that is necessary to maintain the initial pair bond. In the laboratory, the neurobiology of this behavior is studied using resident-intruder testing. Although it is well established that social behaviors in other species are mediated by endogenous opioid systems, opiate regulation of pair bond maintenance has never been studied. Here, we used resident-intruder testing to determine whether endogenous opioids within brain motivational circuitry mediate selective aggression in prairie voles. We first show that peripheral blockade of -opioid receptors with the antagonist norbinaltorphimine (nor-BNI; 100 mg/kg), but not with the preferential -opioid receptor antagonist naloxone (1, 10, or 30 mg/kg), decreased selective aggression in males. We then provide the first comprehensive characterization of -and -opioid receptors in the prairie vole brain. Finally, we demonstrate that blockade of -opioid receptors (500 ng nor-BNI) within the nucleus accumbens (NAc) shell abolishes selective aggression in both sexes, but blockade of these receptors within the NAc core enhances this behavior specifically in females. Blockade of -opioid receptors within the ventral pallidum or -opioid receptors with the specific -opioid receptor antagonist H-D-Phe-Cys-Tyr-D-Trp-Arg-Thr-PenThr-NH2 (1 ng CTAP) within the NAc shell had no effect in either sex. Thus, -opioid receptors within the NAc shell mediate aversive social motivation that is critical for pair bond maintenance.

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Section: Fecundity and Pair Bondingmentioning

confidence: 99%

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

et al. 2012

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“…An occasionally overlooked aspect of their natural history is that while a majority of males and females form bonds and establish socially monogamous breeding units ('residents'), an important minority of prairie voles remains single and traverses large undefended home ranges ('wanderers') [21][22][23]55]. Although the V1aR and OTR profiles of residents and wanderers do not differ among structures involved in the 'pairbonding neural circuit', structures important for socio-spatial memory robustly predict whether residents or wanderers sire offspring [35,36].…”

Section: (B) Protective Influences Of Post-wean Environments On Sociamentioning

confidence: 99%

“…While most breeding units in nature consist of a heterosexual pair (referred to as 'residents') and their offspring, some reproductively active animals are single owing to a member of the pair defecting ('divorce'), predation or what appears to be an active choice to forgo pairbonding [21 -23]. Furthermore, 'wandering' individuals can be male or female [21][22][23][24]. These differences in mating tactics result in natural variation in the postnatal social environment; both parents will raise some offspring, and just mothers will raise others.…”

Section: Introductionmentioning

confidence: 99%

Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

et al. 2015

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Social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. We asked if social experience before and after weaning influenced adult social cognition in male prairie voles. Animals were raised either with or without fathers and then either housed singly or in sibling pairs. Males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social recognition or dissociate spatial from social information. We also examined oxytocin and vasopressin receptors (OTR and V1aR) in areas of the forebrain associated with social behaviour and memory. Pre-and post-wean experience differentially altered receptor expression in several structures. Of note, OTR in the lateral septum-an area in which oxytocin inhibits social recognition-was greatest in animals that did not clearly demonstrate social recognition. The combination of absentee fathers on V1aR in the retrosplenial cortex and single housing on OTR in the septohippocampal nucleus produced a unique phenotype previously found to be associated with poor reproductive success in nature. We demonstrate that interactive effects of early life experiences throughout development have tremendous influence over brain -behaviour phenotype and can buffer potentially negative outcomes due to social deprivation.

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“…There are many cases where apparently monogamous species in fact show high incidences of extra-pair mating, and thus levels of polygamy are high across a broad taxonomic range (Goossens et al, 1998;Liebgold et al, 2006;Ophir et al, 2008;Sefc et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Evidence of polygamy in the socially monogamous Amazonian fish Arapaima gigas (Schinz, 1822) (Osteoglossiformes, Arapaimidae)

Farias

Leão

Almeida³

et al. 2015

Neotrop. ichthyol.

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Arapaima gigas is one of the largest freshwater fishes of the world. It is socially monogamous, forming pairs, constructing a nest and providing parental care. We performed a paternity analysis under three scenarios in captive, semi-natural and natural areas using 10 microsatellite markers. As a positive control, we analyzed three pairs and their offspring isolated individually in artificial breeding ponds (a priori very high probability of monogamy). We then analyzed two samples of offspring from large artificial ponds with multiple adults but only one reproductive pair (a priori high probability of monogamy), two samples from semi-natural breeding station with multiple adults but only one reproductive pair (a priori high probability of monogamy), and a sample from a natural lake with multiple adults, some potentially breeding (a priori medium probability of monogamy). Analysis of patterns of Mendelian heredity suggested an extra-pair contribution for all broods except the positive controls. Similarly, results based on multilocus analysis estimated at least two sib-groups per nest. These results reject monogamy as a system of breeding in Arapaima gigas. From a management perspective, this behavior may be exploited to maintain genetic diversity in captive and as well in wild populations of Arapaima gigas.O pirarucu Arapaima gigas é um dos maiores peixes de água doce do mundo. É socialmente monogâmico, forma casais, constrói ninhos e fornece cuidado parental. Com o objetivo de acessar o sistema de acasalamento do pirarucu, analisamos três cenários: em áreas de cativeiro, semi-naturais e naturais, utilizando 10 marcadores microssatélites. Como controle positivo, analisamos três casais e suas ninhadas isolados em açudes individuais (probabilidade a priori muito alta de monogamia). A seguir, analisamos duas amostras de ninhadas de um açude com vários adultos, mas somente um casal reprodutivo (probabilidade a priori alta de monogamia), duas amostras de estação de criação semi-natural com vários adultos mas somente um casal reprodutivo (probabilidade a priori alta de monogamia), e uma amostra de lago natural com vários adultos alguns potencialmente em fase de reprodução (probabilidade a priori média de monogamia). Análises de padrões mendelianos de hereditariedade sugerem contribuição extra-par para todas as ninhadas, exceto as do controle positivo. Similarmente, resultados baseados em análises multilocus realizadas no programa KINALYZER estimaram pelo menos dois grupos-irmãos por ninhada. Nossos resultados rejeitam a monogamia como sistema de acasalamento em Arapaima gigas. Da perspectiva de manejo, esse comportamento pode ser explorado para manter a diversidade genética em cativeiro assim como em populações naturais de Arapaima gigas.

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Social but not genetic monogamy is associated with greater breeding success in prairie voles

Cited by 113 publications

References 47 publications

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

Evidence of polygamy in the socially monogamous Amazonian fish Arapaima gigas (Schinz, 1822) (Osteoglossiformes, Arapaimidae)

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