Raised without a father: monoparental care effects over development, sexual behavior, sexual reward, and pair bonding in prairie voles

Valera-Marín, Guillermo; Young, Larry J.; Camacho, F.; Paredes, Raúl G.; Rodríguez, Verónica; Díaz, Néstor Fabián; Portillo, Wendy

doi:10.1016/j.bbr.2021.113264

Cited by 12 publications

(12 citation statements)

References 65 publications

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“…Notably, although many of our neuroendocrine findings in comparisons between BPC and MON offspring replicate those of previous findings, 18 our novel findings, drawn from comparisons of MPA females to their BPC and MON conspecifics, help narrow potential routes of investigation and illustrate new ways in which variations in early‐life social structure may influence offspring neuroendocrine development. New evidence suggests that BPC males experience an increase in dopamine turnover in the NAc above that in MON males 46 . Given that both the CeA and NAc were repeatedly implicated in our findings, and given pair‐bond formation requires the integration of social memory and reward, 7 we suggest that future directions should include a deeper exploration of the mesolimbic pathway, including a deeper assessment of dopaminergic projections to the CeA and NAc, as well as additional structures throughout the hippocampus.…”

Section: Discussionmentioning

confidence: 69%

“…Similarly, paternal absence does not result in increased serum corticosterone in adult California mice 43 . Early in development (ie, PND8‐14), mandarin vole pups show elevated levels of serum corticosterone and ACTH 44 ; however, findings from Jia et al 45 show that MON mandarin vole pups are attended to less that BPC pups (as also seen in prairie voles 19,27,46 ); therefore, it remains unclear whether the elevated CORT and ACTH are indicators of stress or metabolic processes related to thermoregulation. In adulthood, serum CORT and ACTH are elevated in female MON mandarin voles, but not in males 47 .…”

Section: Discussionmentioning

confidence: 99%

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Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Rogers

Freeman

Anderson

et al. 2021

J Neuroendocrinology

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Paternal absence can significantly alter bio‐behavioural development in many biparental species. This effect has generally been demonstrated by comparing the development of offspring reared under biparental care with those reared by a single mother. However, studies employing this design conflate two significant modifications to early‐life experience: removal of father‐specific qualities and the general reduction of offspring‐directed care. In the socially monogamous prairie vole (Microtus ochrogaster), the experience of paternal absence without substitution during development inhibits partner preference formation in adulthood, a hallmark of social monogamy, in females and males. Employing alloparents as substitutes for fathers, our previous work demonstrated that paternal absence affects pair‐bond formation in female offspring via reduced quantity of care, although it affects pair‐bond formation in male offspring by means of a missing paternal quality (or qualities). Here, we present evidence that paternal absence (with and without alloparental substitution) may alter the ontogeny of neural oxytocin receptor (OXTR) and/or vasopressin 1a receptor (AVPR1a) distribution in male and female prairie voles. Compared to biparentally reared controls (BPC), male offspring reared in mother only (MON) and maternal‐plus‐alloparental (MPA) conditions show lower densities of OXTR in the central amygdala; and MPA males show lower densities of OXTR in the caudate putamen and nucleus accumbens. Early‐life experience was not associated with differences in AVPR1a density in males. However, MON and MPA females show greater densities of AVPR1a in the medial amygdala than BPC; and MPA females show greater densities of AVPR1a in the ventromedial nucleus of the hypothalamus. We also demonstrate with corticosterone concentrations that MON and MPA offspring are not differentially susceptible to a stressor (ie, social isolation) than BPC offspring. These findings suggest that paternal absence, although likely not a salient early‐life stressor, has neuroendocrine consequences for offspring, some of which may affect partner preference formation.

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Rogers

Freeman

Anderson

et al. 2021

J Neuroendocrinology

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“…The outcomes were heavily influenced by sex, which was not unanticipated given the strongly sexually dimorphic nature of this behavior and its neuroendocrine systems. As others have repeatedly shown [ 71 , 73 , 77 , 94 , 95 ], lack of paternal care adversely impacted pair-bonding with a lack of partner preference observed in both sexes. Moreover, this is the third time that we showed that developmental FM 550 exposure sex-specifically alters pair-bonding [ 57 , 58 ].…”

Section: Discussionmentioning

confidence: 71%

Individual and Combined Effects of Paternal Deprivation and Developmental Exposure to Firemaster 550 on Socio-Emotional Behavior in Prairie Voles

Gillera

Marinello

Nelson

et al. 2022

Toxics

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The prevalence of neurodevelopmental disorders (NDDs) is rapidly rising, suggesting a confluence of environmental factors that are likely contributing, including developmental exposure to environmental contaminants. Unfortunately, chemical exposures and social stressors frequently occur simultaneously in many communities, yet very few studies have sought to establish the combined effects on neurodevelopment or behavior. Social deficits are common to many NDDs, and we and others have shown that exposure to the chemical flame retardant mixture, Firemaster 550 (FM 550), or paternal deprivation impairs social behavior and neural function. Here, we used a spontaneously prosocial animal model, the prairie vole (Microtus ochrogaster), to explore the effects of perinatal chemical (FM 550) exposure alone or in combination with an early life stressor (paternal absence) on prosocial behavior. Dams were exposed to vehicle (sesame oil) or 1000 µg FM 550 orally via food treats from conception through weaning and the paternal absence groups were generated by removing the sires the day after birth. Adult offspring of both sexes were then subjected to open-field, sociability, and a partner preference test. Paternal deprivation (PD)-related effects included increased anxiety, decreased sociability, and impaired pair-bonding in both sexes. FM 550 effects include heightened anxiety and partner preference in females but reduced partner preference in males. The combination of FM 550 exposure and PD did not exacerbate any behaviors in either sex except for distance traveled by females in the partner preference test and, to a lesser extent, time spent with, and the number of visits to the non-social stimulus by males in the sociability test. FM 550 ameliorated the impacts of parental deprivation on partner preference behaviors in both sexes. This study is significant because it provides evidence that chemical and social stressors can have unique behavioral effects that differ by sex but may not produce worse outcomes in combination.

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“…Moreover, certain developmental environments can influence a male's decision to bond. For example, males raised by a single parent (mothers only) show delayed partner preference formation in adulthood when compared to biparentally raised animals [Ahern and Young, 2009;Valera-Marín et al, 2021]. Very recently, we have found that uniparental or biparental rearing environments also appear to shape mating tactics as assessed by space use in adult males, whereby uniparentally raised males demonstrate larger (wanderer-like) home ranges and are more likely to be wanderers than biparentally raised males living in seminatural field conditions [Madrid et al, unpubl.…”

Section: Individual Level Effectsmentioning

confidence: 99%

“…Indeed, cues associated with female prairie vole fertility and sexual receptivity appear to inform male prairie voles about the potential payoffs of forming a pair bond at that moment with a given potential partner. For instance, males appear to be sensitive to female chemical sexual signals, investi-gating the dirty bedding of receptive females more than bedding from other males or clean bedding [Valera-Marín et al, 2021]. Lesions of the vomeronasal organ, an organ important for processing sexual cues in rodents, greatly reduces reproductive performance in males, with only 22% of lesioned males siring offspring compared to 75% of intact males [Wekesa and Lepri, 1994].…”

Section: Individual Level Effectsmentioning

confidence: 99%

Multi-Level Effects Driving Cognitive and Behavioral Variability among Prairie Voles: Insights into Reproductive Decision-Making from Biological Levels of Organization

Forero

Ophir²

2022

Brain Behav Evol

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Behavioral phenotypes play an active role in maximizing fitness and shaping the evolutionary trajectory of species by offsetting the ecological and social environmental factors individuals experience. How these phenotypes evolve and how they are expressed is still a major question in ethology today. In recent years, an increased focus on the mechanisms that regulate the interactions between an individual and its environment has offered novel insights into the expression of alternative phenotypes. In this review, we explore the proximate mechanisms driving the expression of alternative reproductive phenotypes in the male prairie vole (Microtus ochrogaster) as one example of how the interaction of an individual’s social context and internal milieu has the potential to alter behavior, cognition, and reproductive decision-making. Ultimately, integrating the physiological and psychological mechanisms of behavior advances understanding into how variation in behavior arises. We take a “levels of biological organization” approach, with prime focus placed on the level of the organism to discuss how cognitive processes emerge as traits, and how they can be studied as important mechanisms driving the expression of behavior.

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Raised without a father: monoparental care effects over development, sexual behavior, sexual reward, and pair bonding in prairie voles

Cited by 12 publications

References 65 publications

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Individual and Combined Effects of Paternal Deprivation and Developmental Exposure to Firemaster 550 on Socio-Emotional Behavior in Prairie Voles

Multi-Level Effects Driving Cognitive and Behavioral Variability among Prairie Voles: Insights into Reproductive Decision-Making from Biological Levels of Organization

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