Opposite effects of nonapeptide antagonists on paternal behavior in the teleost fish Amphiprion ocellaris

DeAngelis, Ross; Gogola, Joseph V.; Dodd, Logan; Rhodes, Justin S.

doi:10.1016/j.yhbeh.2017.02.013

Cited by 37 publications

(24 citation statements)

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“…Strategic comparisons of social behavioral divergence at the species and population levels have discovered causal genetic and neurobiological mechanisms contributing to specific social behaviors (Bendesky et al, 2017; Goodson et al, 2009; Greenwood et al, 2016; Haesler et al, 2007; Haesler et al, 2004; Insel & Shapiro, 1992; Insel et al, 1994; Kowalko et al, 2013; Lim et al, 2004). For example, investigations in alternative species systems spanning teleost fishes and mammals have begun to reveal the roles of brain-region specific OT and AVP receptor (OTR and V1aR, respectively) populations in modulating species-specific social behaviors (DeAngelis et al, 2017; Donaldson & Young, 2008; Goodson & Bass, 2000; Keebaugh et al, 2015; O’Connell et al, 2012; Oldfield & Hofmann, 2011; Song et al, 2014). Comparative investigations followed by causal manipulations and have demonstrated the role of region-specific OTR and V1aR populations in modulating flocking behavior in Estrildidae finches and pair bonding behavior in Microtine voles (Goodson et al, 2009; Insel & Shapiro, 1992; Insel et al, 1994; Lim et al, 2004; Young et al, 2001).…”

Section: Patterns Of Social Behavioral Variation In Naturementioning

confidence: 99%

“…Strategic comparisons at the species and population levels in non-traditional organisms have discovered causal genetic and neurobiological mechanisms contributing to natural variation in social behavior (Insel & Shapiro 1992;Insel et al 1994;Haesler et al 2004Haesler et al , 2007Goodson et al 2009;Kowalko et al 2013;Greenwood et al 2016;Bendesky et al 2017). For example, investigations in alternative species systems spanning teleost fishes and mammals have begun to reveal the roles of brain-region specific OT and AVP receptor (OTR and V1aR, respectively) populations in modulating species-specific social behaviors (Goodson & Bass 2000;Donaldson & Young 2008;Oldfield & Hofmann 2011;O'Connell et al 2012;Song et al 2014;Keebaugh et al 2015;DeAngelis et al 2017). Follow-up pharmacological manipulations have demonstrated the causal roles of region-specific OTR and V1aR populations in modulating flocking behavior in Estrildidae finches and pair bonding behavior in Microtine voles (Insel & Shapiro 1992;Insel et al 1994;Young et al 2001;Goodson et al 2009).…”

Section: Rapid Evolutionary Divergence Of Social Behaviorsmentioning

confidence: 99%

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Evolutionary diversity as a catalyst for biological discovery

Johnson

Young

2018

Integrative Zoology

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The tremendous diversity of animal behaviors has inspired generations of scientists from an array of biological disciplines. To complement investigations of ecological and evolutionary factors contributing to behavioral evolution, modern sequencing, gene editing, computational and neuroscience tools now provide a means to discover the proximate mechanisms upon which natural selection acts to generate behavioral diversity. Social behaviors are motivated behaviors that can differ tremendously between closely related species, suggesting phylogenetic plasticity in their underlying biological mechanisms. In addition, convergent evolution has repeatedly given rise to similar forms of social behavior and mating systems in distantly related species. Social behavioral divergence and convergence provides an entry point for understanding the neurogenetic mechanisms contributing to behavioral diversity. We argue that the greatest strides in discovering mechanisms contributing to social behavioral diversity will be achieved through integration of interdisciplinary comparative approaches with modern tools in diverse species systems. We review recent advances and future potential for discovering mechanisms underlying social behavioral variation; highlighting patterns of social behavioral evolution, oxytocin and vasopressin neuropeptide systems, genetic/transcriptional "toolkits," modern experimental tools, and alternative species systems, with particular emphasis on Microtine rodents and Lake Malawi cichlid fishes.

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Section: Patterns Of Social Behavioral Variation In Naturementioning

confidence: 99%

Section: Rapid Evolutionary Divergence Of Social Behaviorsmentioning

confidence: 99%

Evolutionary diversity as a catalyst for biological discovery

Johnson

Young

2018

Integrative Zoology

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“…The melanocortin system involving the POMC genes have been shown to be directly related to cichlid behavior where yellow Astatotilapia burtoni males were more aggressive and had lower cortisol levels than the blue males [15]. Both AVP and OXT genes contain similar nonapeptides, isotocin (homologous to mammalian oxytocin) and vasotocin (homologous to mammalian vasopressin), respectively, that influence various fish social behaviors [8,11,[16][17][18][19][20][21]. AVP has been associated with a variety of fish behaviors, including social status [22,23], and regulates mate-guarding behaviors [24] and species differences in mutualistic behavior [25].…”

Section: Introductionmentioning

confidence: 99%

Characterization of the prohormone complement in Amphiprion and related fish species integrating genome and transcriptome assemblies

et al. 2020

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The Amphiprion (anemonefish or clownfish) family of teleost fish, which is not a common model species, exhibits multiple unique characteristics, including social control of body size and protandrous sex change. The social changes in sex and body size are modulated by neuropeptide signaling pathways. These neuropeptides are formed from complex processing from larger prohormone proteins; understanding the neuropeptide complement requires information on complete prohormones sequences. Genome and transcriptome information within and across 22 teleost fish species, including 11 Amphiprion species, were assembled and integrated to achieve the first comprehensive survey of their prohormone genes. This information enabled the identification of 175 prohormone isoforms from 159 prohormone proteins across all species. This included identification of 9 CART prepropeptide genes and the loss of insulin-like 5B and tachykinin precursor 1B genes in Pomacentridae species. Transcriptome assemblies generally detected most prohormone genes but provided fewer prohormone genes than genome assemblies due to the lack of expression of prohormone genes or specific isoforms and tissue sampled. Comparisons between duplicate genes indicated that subfunctionalization, degradation, and neofunctionalization may be occurring between all copies. Characterization of the prohormone complement lays the foundation for future peptidomic investigation of the molecular basis of social physiology and behavior in the teleost fish.

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“…OT-like compounds facilitate male parental care in several non-mammalian species [(14, 15); c.f. (16)].…”

Section: Introductionmentioning

confidence: 99%

“…Similarly, V1aR mRNA is downregulated in biparental California mouse fathers, and increased V1aR mRNA expression in California mice is associated with longer latencies to approach pups (28). AVP-mediated inhibition of paternal behavior is present in non-mammals as well; intraperitoneal vasotocin inhibited paternal behavior in poison frogs and clownfish (14, 16). In other contexts, the relationship between AVP and caregiving behavior by non-mothers is less clear.…”

Section: Introductionmentioning

confidence: 99%

Vasopressin and Oxytocin Reduce Food Sharing Behavior in Male, but Not Female Marmosets in Family Groups

2017

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Oxytocin (OT) is critical for lactation and maternal care, but OT and the related nonapeptide vasopressin are important for caregiving behaviors in fathers and alloparents as well. This experiment tested the effects of vasopressin and OT on food sharing in marmoset families. We treated caregivers (parents, siblings) with intranasal vasopressin, OT, or saline, and then paired them with the youngest marmoset in the family. Caregivers were given preferred food, and then observed for food sharing and aggressive behavior with young marmosets. OT reduced food sharing from male alloparents to youngest siblings, and fathers that received vasopressin refused to share food with their youngest offspring more often than when treated with OT. Vasopressin increased aggressive vocalizations directed toward potential food recipients in all classes of caregivers. These results indicate that vasopressin and OT do not always enhance prosocial behavior: modulation of food sharing depends on both sex and parental status.

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Opposite effects of nonapeptide antagonists on paternal behavior in the teleost fish Amphiprion ocellaris

Cited by 37 publications

References 44 publications

Evolutionary diversity as a catalyst for biological discovery

Evolutionary diversity as a catalyst for biological discovery

Characterization of the prohormone complement in Amphiprion and related fish species integrating genome and transcriptome assemblies

Vasopressin and Oxytocin Reduce Food Sharing Behavior in Male, but Not Female Marmosets in Family Groups

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