An official website of the United States government
Abstract 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.
more »
« less
Paternal exposure to a common pharmaceutical (Ritalin) has transgenerational effects on the behaviour of Trinidadian guppies
Abstract Evidence is emerging that paternal effects, the nongenetic influence of fathers on their offspring, can be transgenerational, spanning several generations. Methylphenidate hydrochloride (MPH; e.g. Ritalin) is a dopaminergic drug that is highly prescribed to adolescent males for the treatment of Attention-deficit/hyperactivity disorder. It has been suggested that MPH could cause transgenerational effects because MPH can affect the male germline in rodents and because paternal effects have been observed in individuals taking similar drugs (e.g. cocaine). Despite these concerns, the transgenerational effects of paternal MPH exposure are unknown. Therefore, we exposed male and female Trinidadian guppies ( Poecilia reticulata ) to a low, chronic dose of MPH and observed that MPH affected the anxiety/exploratory behaviour of males, but not females. Because of this male-specific effect, we investigated the transgenerational effects of MPH through the paternal line. We observed behavioural effects of paternal MPH exposure on offspring and great-grandoffspring that were not directly administered the drug, making this the first study to demonstrate that paternal MPH exposure can affect descendants. These effects were not due to differential mortality or fecundity between control and MPH lines. These results highlight the transgenerational potential of MPH.
more »
« less
- Award ID(s):
- 1740466
- PAR ID:
- 10325269
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Behavioral traits are often the first response to changing environmental conditions, including human induced rapid environmental change. For example, animals living in urban areas are often more aggressive than rural animals. This is especially evident in songbirds; males of several species display elevated aggression in urban habitats. Increased male aggression has been associated with reduced parental care, but the consequences of this trade-off for males, social partners, and offspring in the context of urbanization remains unclear. We explored the effects of increased urban male aggression on the life history traits, parental care, and offspring outcomes of song sparrows (Melospiza melodia). We predicted that urban males would reduce paternal investment and result in urban females providing greater nestling care or reduced fledging success in urban habitats compared to rural. Contrary to our prediction, aggressive urban males did not decrease care but visited the nest more often compared to rural males. Additionally, urban birds had higher nest and fledging success compared to rural, though this was largely due to higher nest predation in rural habitats. Our study is among the first to evaluate trade-offs associated with elevated aggression expressed by urban animals and adds to a growing body of evidence that urban habitats provide benefits to some species.more » « less
-
When female chimpanzees, orangutans, and callitrichids share challenging‐to‐process resources with their offspring, they improve offspring access to foods and calories which would otherwise be unavailable. Adult chimpanzees share foods rarely, but when they do, sharing valuable resources solidifies inter‐individual bonds (e.g., when building coalitions or eliciting copulations). While maternal‐offspring food sharing has been studied in wild orangutans, the context in which adult orangutans share food and feed in proximity is poorly known. We use 27 years of research on orangutans in West Kalimantan, Indonesia, to examine this behavior. Food sharing and tolerance were observed during 2,131 follows between 1994‐2019. Mother‐infant food sharing occurred in 78%, of these follows, female‐female sharing in 22%, male‐female sharing in 32%, and male‐male in just 1%. Adult females shared foods at different rates with adult males than with offspring (Chi‐square = 49.27,p< .01,N= 589 events). Eighty‐one percent of mother‐offspring food sharing/tolerance was fruit, compared to only 71% of male‐female food sharing/tolerance. Durio, Lithocarpus, and Willughbeia (hard‐to‐process fruits) were most frequently shared by mothers. Twenty‐three percent of male‐female food sharing/tolerance occurred while eating termites; only 3% of mother‐infant sharing did. Only two of 350 mouth‐to‐mouth or hand‐to‐mouth transfers involved adult males and females. Mothers increase their offspring’s access to challenging resources, while food sharing/tolerance among adult males and females is not limited to valuable resources, but may indicate strong social tolerance or affiliation in generally solitary adultsmore » « less
-
BackgroundEnhancing an organism’s survival hinges on the development of balanced and adaptable stress response systems. While the initial stress-response set-points in the hypothalamus may be genetically determined, they are further influenced by epigenetic factors during embryonic development. A debate persists regarding the heritability of such behavioral traits. The chickin ovoheat conditioning model offers a unique insight into this fundamental question, where manipulation during embryonic development can induce heat resilience and even cross-tolerance to promote immunological resilience. In this study, we conducted an analysis of thermal manipulation during embryogenesis to demonstrate paternal heredity and investigate its transmission through sperm DNA methylation in coordination with miR-200a action. ResultFirst-generation embryos underwentin ovoheat conditioning (EHC), creating a cohort of embryonic EHC and control chicks. These chicks were then subjected to an intracranial lipopolysaccharide (LPS) challenge. Conditioning rendered the chicks immune resilient, as evidenced by their fibril effect. Male offspring were raised to maturity, and their sperm was analyzed for methylome patterns, revealing significant differences between treatments, particularly in immune and development related genes. Additionally, sperm from EHC males was used for artificial insemination of naïve Cobb hens, resulting in untreated offspring that displayed immune resilience upon LPS challenge, indicating transgenerational effects. Overlap analysis of sperm methylome and differentially methylated sites (DMS) of offspring hypothalamus revealed inheritance of altered methylation associated with specific genes. Several of these genes are potential effectors of miR-200a, whose expression profile in the hypothalamus during LPS challenge was conserved across both generations. To evaluate the role of miR-200a in cross-tolerance acquisition, miR-200a was intracranially injected, and RNA-seq analysis of the hypothalamus revealed genes involved in the regulation of developmental and metabolic processes, stress, and immune response. ConclusionThis study demonstrates paternal trait heredity by revealing that EHC induces cross-tolerance with the immunological system, rendering chicks resilient to LPS that transgenerationally transmit this to untreated offspring. Additionally, analysis of sperm methylation patterns in EHC mature chicks led to identification of genes associated with neuronal development and immune response, indicating potential neural network reorganization. Finally, miR-200a emerges as a regulator potentially involved in mediating the cross-tolerance effect.more » « less
-
The prevalence of chronic inflammation increases with age and may be aggravated by environmental exposures. Similarly, during immune aging, inflammatory disease incidence increases as protective immunity decreases. To better understand disease and exposure risks, an immune aging model outlining key changes in immune function is crucial. Utilizing the lowest possible vertebrate class, we propose the Japanese medaka (Oryzias latipes) as a model to investigate sex-specific immune aging including changes in immune gene expression, leukocyte profiles, and organismal level immune response. Evaluating the expression of immune initiators (CRP, TLR5-s, TLR5-m, TCRb, and MHCII), immune mediators (MYD88, Nf-kß, C3, and IL1b), and immune effectors (LYZ and C8) in concomitance with alterations in leukocyte populations and host resistance to pathogens will inform about immune competence across ages. The data presented here demonstrate a critical decrease in the expression of immune initiators (CRP, TLR5-soluble, TCRb, and MHCII), mediators (MYD88, Nf-kß, C3, and IL1b), and effector (LYZ) in both females and males after 11 months post hatching (mph). Interestingly, both sexes displayed an upregulation for the immune effector, C8, during this older life stage (11–13 mph). Gene expression profiles for both sexes at the most elderly age (20 or 23 mph) appear to revert to a younger profile of expression indicating a second change in immune function during aging rather than a steady decline. Significant changes in leukocyte populations were observed in both male and female medaka after peaking sexual maturation at 3 mph. Organismal level immune competence data revealed male medaka at the elderly age to be more vulnerable than their female and younger male counterparts while no differences were observed in females based on age. Together, these data provide a holistic profile for immune aging in medaka, a useful tool for future immunological studies considering age as a factor influencing disease susceptibility.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41598-021-83448-x
