Paternal retrievals increase testosterone levels in both male and female California mouse (Peromyscus californicus) offspring

Chary, Mamatha; Cruz, Jayson P.; Bardi, Massimo; Becker, Elizabeth A.

doi:10.1016/j.yhbeh.2015.05.013

Cited by 11 publications

(13 citation statements)

References 55 publications

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“…After collection, samples were centrifuged and separated, then stored at −80°C until assayed. Plasma T (1:10 dilution) and Cort (1:50 dilution) concentrations were determined using commercial assay kits (Enzo Life Sciences, Farmingdale, NY, USA) previously validated in the California mouse (Chary et al, 2015). The standard curve slope generated for Cort had a slope of 1 ( r 2 = 0.91) and the slope for T was 0.72 ( r 2 = 0.87).…”

Section: Methodsmentioning

confidence: 99%

“…We hypothesized that PVN and SON OT-ir would be higher in HC than LC offspring. Since California mouse pups experience transient increases in T following paternal retrievals (Becker et al, 2010; Chary et al, 2015) and postnatal surges in T lead to higher adult T levels (Sachser and Proöve, 1988; Lürzel et al, 2010), we predicted higher basal T levels in adult HC than LC offspring. Lastly, as a manipulation check, we measured basal Cort levels to confirm that our modified retrieval manipulation had no lasting effects on stress reactivity; predicting similar basal Cort levels between HC and LC offspring.…”

Section: Introductionmentioning

confidence: 99%

“…Within the bi-parental California mouse ( Peromyscus californicus ), fathers provide high-care (HC) towards both same and opposite sex offspring, which influence neuroendocrine mechanisms that facilitate similar rather than sexually dimorphic development. Transient increases in testosterone levels (Becker et al, 2010; Chary et al, 2015) and greater arginine vasopressin (AVP) expression in the bed nucleus of the stria terminalis (BNST; Frazier et al, 2006; Yohn et al, 2017), accompany territorial aggression in HC offspring. Whereas in most species parental behavior is accompanied by a reduction in aggression and T, in bi-parental species (Hume and Wynne-Edwards, 2005), like the territorial California mouse (Trainor and Marler, 2001, 2002), T remains high in fathers and is important for maintaining paternal behavior since castration reduces paternal behavior in this species (Trainor and Marler, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…For example, California mouse offspring experience transient increases in T in response to paternal retrievals (Becker et al, 2010; Chary et al, 2015). It is possible that experiencing these brief increases in T will result in overall increased basal T levels in adulthood since postnatal T is correlated with adult T (Sachser and Proöve, 1988; Lürzel et al, 2010), although this hypothesis has yet to be tested.…”

Section: Introductionmentioning

confidence: 99%

“…Additionally, paternal deprivation leads to deficits in social behavior (Yu et al, 2012; Bambico et al, 2015) and increased anxiety (McEwen, 2007; Roberts et al, 2007; Jia et al, 2009; Kim et al, 2013), which may correlate with HPA dysregulation since in response to stress, corticosterone (Cort) is secreted. However, no transient differences in Cort in response to paternal care (Becker et al, 2010; Chary et al, 2015) nor basal Cort dissimilarities between paternal absence or presence (Wang et al, 2012) have been reported.…”

Section: Introductionmentioning

confidence: 99%

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Paternal Care Impacts Oxytocin Expression in California Mouse Offspring and Basal Testosterone in Female, but Not Male Pups

Yohn

Leithead

Ford

et al. 2018

Front. Behav. Neurosci.

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Natural variations in parenting are associated with differences in expression of several hormones and neuropeptides which may mediate lasting effects on offspring development, like regulation of stress reactivity and social behavior. Using the bi-parental California mouse, we have demonstrated that parenting and aggression are programmed, at least in part, by paternal behavior as adult offspring model the degree of parental behavior received in development and are more territorial following high as compared to low levels of care. Development of these behaviors may be driven by transient increases in testosterone following paternal retrievals and increased adult arginine vasopressin (AVP) immunoreactivity within the bed nucleus of the stria terminalis (BNST) among high-care (HC) offspring. It remains unclear, however, whether other neuropeptides, such as oxytocin (OT), which is sensitive to gonadal steroids, are similarly impacted by father-offspring interactions. To test this question, we manipulated paternal care (high and low care) and examined differences in adult offspring OT-immunoreactive (OT-ir) within social brain areas as well as basal T and corticosterone (Cort) levels. HC offspring had more OT-ir within the paraventricular nucleus (PVN) and supraoptic nucleus (SON) than low-care (LC) offspring. Additionally, T levels were higher among HC than LC females, but no differences were found in males. There were no differences in Cort indicating that our brief father-pup separations likely had no consequences on stress reactivity. Together with our previous work, our data suggest that social behavior may be programmed by paternal care through lasting influences on the neuroendocrine system.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Paternal Care Impacts Oxytocin Expression in California Mouse Offspring and Basal Testosterone in Female, but Not Male Pups

Yohn

Leithead

Ford

et al. 2018

Front. Behav. Neurosci.

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Revisiting paternal absence: Female alloparental replacement of fathers recovers partner preference formation in female, but not male prairie voles (Microtus ochrogaster)

Rogers

Bales

2019

Developmental Psychobiology

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In prairie voles (Microtus ochrogaster), biparental care of offspring is typical, and paternal absence in the pre‐weaning development of offspring alters biobehavioral development. We sought to determine whether this altered development is due to the absence of specific paternal qualities or a general reduction in pup‐directed care. We compared the biobehavioral development of pups reared under conditions of biparental (BPC), maternal‐plus‐alloparental (MPA; i.e., mother and older sister), and maternal only (MON) care. Older sisters provided a quantity of care equal to or greater than that of fathers. Growth rate and developmental milestones were unaffected by family composition, with the exception of earlier fur growth in MON conditions. In adulthood, we tested behaviors on an elevated plus maze, spontaneous alloparental care, and partner preference formation. We found no significant differences on the elevated plus maze and only marginal differences in alloparental care. While both female and male MON individuals showed deficits in partner preference formation, MPA females showed typical partner preference formation. However, the alloparental substitution of fathers was not sufficient for the typical development of partner preference formation in males. We conclude that paternal care plays a differentially important role in the social development of female and male prairie vole offspring.

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Transmission of paternal retrieval behavior from fathers to sons in a biparental rodent

Becker

Leithead

Libo

et al. 2021

Developmental Psychobiology

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Transmission of maternal behavior across generations occurs, but less is known about paternal behavior. In biparental species like the California mouse (Peromyscus californicus), paternal care contributes to the well‐being of offspring with lasting consequences on the brain and behavior. Paternal huddling/grooming behavior can be passed on to future generations, but whether paternal retrieval, which removes young from potential harm, is transmitted independently is unclear. We manipulated paternal retrieval experience through pup displacement manipulations, then examined whether males exposed to higher levels of paternal retrieval in development altered their adult retrieval behavior with their offspring. Males exposed to heightened paternal retrievals, as compared to reduced retrievals, retrieved their offspring more often but huddled/groomed offspring less during undisturbed natural observations. No differences were observed following a pup displacement challenge. The high paternal retrieval group also exhibited more physical activity and stereotypy. Our results are consistent with the hypothesis that paternal retrieval levels are transmitted across generations and may function via mechanisms separate from huddling/grooming. One modifying factor may be anxiety because increased activity and stereotypy occurred in the high retrieval group. We speculate how the transmission of paternal retrievals may inform a protective parenting style.

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Paternal retrievals increase testosterone levels in both male and female California mouse (Peromyscus californicus) offspring

Cited by 11 publications

References 55 publications

Paternal Care Impacts Oxytocin Expression in California Mouse Offspring and Basal Testosterone in Female, but Not Male Pups

Paternal Care Impacts Oxytocin Expression in California Mouse Offspring and Basal Testosterone in Female, but Not Male Pups

Revisiting paternal absence: Female alloparental replacement of fathers recovers partner preference formation in female, but not male prairie voles (Microtus ochrogaster)

Transmission of paternal retrieval behavior from fathers to sons in a biparental rodent

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