Neurogenomic insights into paternal care and its relation to territorial aggression

Bukhari, Syed; Saul, Michael C.; James, Noelle; Bensky, Miles K.; Stein, Laura R.; Trapp, Rebecca; Bell, Alison M.

doi:10.1038/s41467-019-12212-7

Cited by 36 publications

(23 citation statements)

References 64 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…DEGs between adjacent fighting stages, i.e., D20 and D60, D60 and A0, and A0 and A30, were referred to as transitional genes, which might be involved in facilitating the transition into the next fighting stage, priming for and/or responding to a particular event or stimulus during that fighting stage, e.g., a shift in social status. In addition, we used a more stringent criterion than was used in the analysis of Fig (27,42), suggesting that some of the molecular mechanisms of aggressive behavior might be deeply conserved.…”

Section: S5 Fig) Those Sharedmentioning

confidence: 99%

“…The fighting process in B. splendens proceeds in a stereotypic manner, beginning with each fish displaying their fins and circling, followed by their performing a series of biting/striking/mouthlocking/chasing behaviors, and ending when one opponent shows fleeing/freezing behavior indicating surrender (26). Thus, one might expect that each fighting stage could have unique gene expression data associated with it (i.e., unique hypothesis) (27). Moreover, there are transient periods between these fighting stages, and some of the aggressive behaviors remain constant across stages, e.g., chasing.…”

Section: Introductionmentioning

confidence: 99%

“…Thus, one might also expect to see that the brain transcription signal of a preceding fighting stage persists into subsequent stages, resulting in shared gene expression among fighting stages in the series. The expression of these genes would thus be either transient between temporally adjacent stages in the series or persistent across all fighting stages (i.e., carryover hypothesis) (27). Although these hypotheses help to improve our understanding of aggressive confrontation at the molecular level, we know little about which genes conform to a unique or carryover pattern across stages of fighting.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

A unique neurogenomic state emerges after aggressive confrontations in males of the fishBetta splendens

Iwasaki

Oshima

et al. 2020

Preprint

View full text Add to dashboard Cite

Territorial defense involves frequent aggressive confrontations with competitors, but little is known about how brain-transcriptomic profiles change between individuals competing for territory establishment. Our previous study elucidated that brain-transcriptomic synchronization occurs in a pair-specific manner between two males of the fish Betta splendens during fighting, reflecting a mutual assessment process between them at the level of gene expression. Here we evaluated how the brain-transcriptomic profiles of opponents change immediately after shifting their social status (i.e., the winner/loser has emerged) and 30 min after this shift. We showed that unique and carryover hypotheses can be adapted to this system, in which changes in the expression of certain genes are unique to different fighting stages and in which the expression patterns of certain genes are transiently or persistently changed across all fighting stages. Interestingly, the specificity of the brain-transcriptomic synchronization of a pair during fighting was gradually lost after fighting ceased, because of the decrease in the variance in gene expression across all individuals, leading to the emergence of a basal neurogenomic state. Strikingly, this unique state was more basal than the state that existed in the before-fighting group and resulted in the reduced and consistent expression of genes across all individuals. In spite of the consistent and basal overall gene expression in each individual in this state, expression changes for genes related to metabolism, learning and memory, and autism still differentiated losers from winners. The fighting system using male B. splendens thus provides a promising platform for investigating neurogenomic states of aggression in vertebrates.Author summaryCompetitive interactions involve complex decision-making tasks that are shaped by mutual feedback between participants. When two animals interact, transcriptomes across their brains synchronize in a way that reflects how they assess and predict the other’s fighting ability and react to each other’s decisions. Here, we elucidated the gradual loss of brain-transcriptomic synchrony between interacting opponents after their interaction ceased, leading to the emergence of a basal neurogenomic state, in which the variations in gene expression were reduced to a minimum among all individuals. This basal neurogenomic state shares common characteristics with the hibernation state, which animals adopt to minimize their metabolic rates to cope with harsh environmental conditions. We demonstrated that this unique neurogenomic state, which is newly characterized in the present study, is composed of the expression of a unique set of genes, each of which was presumably minimally required for survival, providing a hypothesis that this state represents the smallest unit of neurogenomic activity for sustaining an active life.

show abstract

Section: S5 Fig) Those Sharedmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A unique neurogenomic state emerges after aggressive confrontations in males of the fishBetta splendens

Iwasaki

Oshima

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…IRF5 is produced in the brain by microglia (resident immune cells in the brain) and it is known for its pro-inflammatory functions [51,52]. Extensive neuroimmune changes occur in rodents postpartum (reviewed in [53]) and it is likely that some of these extend to other vertebrate species (e.g., [54]).…”

Section: (C) What Neural Changes Are Associated With Spontaneous Care?mentioning

confidence: 99%

Brain transcriptomic changes in Japanese quail reveal roles for neurotensin and urocortin 3 in avian parental care

Lopes

Bruijn

2020

Preprint

View full text Add to dashboard Cite

For many species, parental care critically affects offspring survival. But what drives animals to display parental behaviours towards young? In mammals, pregnancy-induced physiological transformations seem key in preparing the neural circuits that lead towards attraction (and reduced-aggression) to young. Beyond mammalian maternal behaviour, knowledge of the neural mechanisms that underlie parental care is severely lacking. We took advantage of a domesticated bird species, the Japanese quail, for which parental behaviour towards chicks can be induced through a sensitization procedure, a process that is not effective in all animals. We used the variation in parental responses to study neural transcriptomic changes associated with the sensitization procedure itself, with the outcome of the procedure (i.e., presence of parental behaviours) and with spontaneous parental care (i.e., in the absence of sensitization). Out of the brain regions studied, we found that most differences in gene expression were located in the hypothalamus. Our results highlight several molecular pathways that may contribute to the modulation of avian parental care. We identified one gene, neurotensin, that was previously only demonstrated to be causally associated with parental care in mammals. Our work opens new avenues of research into understanding the neural basis of parental care in non-mammalian species.

show abstract

“…A well-known example is the dramatic change in brain morphology and gene expression that occurs to promote singing behavior as the breeding season begins [8, 9]. The neurogenomic shift from non-breeding to breeding states has been relatively well-studied using both targeted gene approaches [10–12] and genome-wide studies [13, 14], but the shift from early breeding stages to later parental stages has received far less attention [15]. Moreover, past work examining changes within the breeding season, as males adjust to parental demands, has primarily focused on steroidogenic genes [16–18].…”

Section: Introductionmentioning

confidence: 99%

The neurogenomic transition from territory establishment to parenting in a territorial female songbird

et al. 2019

View full text Add to dashboard Cite

BackgroundThe brain plays a critical role in upstream regulation of processes central to mating effort, parental effort, and self-maintenance. For seasonally breeding animals, the brain is likely mediating trade-offs among these processes within a short breeding season, yet research thus far has only explored neurogenomic changes from non-breeding to breeding states or select pathways (e.g., steroids) in male and/or lab-reared animals. Here, we use RNA-seq to explore neural plasticity in three behaviorally relevant neural tissues (ventromedial telencephalon [VmT], hypothalamus [HYPO], and hindbrain [HB]), comparing free-living female tree swallows (Tachycineta bicolor) as they shift from territory establishment to incubation. We additionally highlight changes in aggression-related genes to explore the potential for a neurogenomic shift in the mechanisms regulating aggression, a critical behavior both in establishing and maintaining a territory and in defense of offspring.ResultsHB had few differentially expressed genes, but VmT and HYPO had hundreds. In particular, VmT had higher expression of genes related to neuroplasticity and processes beneficial for competition during territory establishment, but down-regulated immune processes. HYPO showed signs of high neuroplasticity during incubation, and a decreased potential for glucocorticoid signaling. Expression of aggression-related genes also shifted from steroidal to non-steroidal pathways across the breeding season.ConclusionsThese patterns suggest trade-offs between enhanced activity and immunity in the VmT and between stress responsiveness and parental care in the HYPO, along with a potential shift in the mechanisms regulating aggression. Collectively, these data highlight important gene regulatory pathways that may underlie behavioral plasticity in females.

show abstract

Neurogenomic insights into paternal care and its relation to territorial aggression

Cited by 36 publications

References 64 publications

A unique neurogenomic state emerges after aggressive confrontations in males of the fishBetta splendens

A unique neurogenomic state emerges after aggressive confrontations in males of the fishBetta splendens

Brain transcriptomic changes in Japanese quail reveal roles for neurotensin and urocortin 3 in avian parental care

The neurogenomic transition from territory establishment to parenting in a territorial female songbird

Contact Info

Product

Resources

About