Teleost Dominance Hierarchies

Cross references:     Dominance Hierarchies in General    Fish    
Osteichthyes (Bony Fish)     Teleosts     Teleost Hormones     Teleost Cortisol, etc.    Male Dominance Hierarchy     Cortisol & Dominance  


FINAL SUMMARY
OF FIVE REFERENCES
1991 - 2008


    "... nonterritorial males have lower levels of Testosterone (T) and 11KT than territorial males.  Nonterritorial males allowed access to vacant territories underwent pronounced increases in T and 11KT."  
    The endocrine data are consistent with activity of either the Direct Serotonin Pathway  or the    Indirect Serotonin Pathway  or both acting simultaneously.    
 


INITIAL SUMMARIES
OF THE REFERENCES

Following are initial summaries of the references.  The references are designated by the first words of their title and their year of publication.   

The references themselves follow this list of their initial summaries. 


Androgen control of social status in males ... - 1991 
     "... nonterritorial males have lower levels of Testosterone (T) and 11KT than territorial males.  Nonterritorial males allowed access to vacant territories underwent pronounced increases in T and 11KT."  
 

Effect of dominance status ...  - 1996  
    " In small groups of rainbow trout (Onchorhynchus mykiss) spawning in the laboratory,  Dominant males had higher plasma levels of Testosterone (T) ... compared with subordinates.


Serotonin as a regulator ...   - 1997   
    "The anatomical organization of the brain serotonergic systems is remarkably conserved among vertebrates, implicating that 5-HT functions might also have been conserved.
    ... In a number of teleost species as well as in mammals, social  subordination and other stressors, including handling and predator exposure, elevates brain 5-HT activity ..."   


Elevation of brain 5-HT activity ...  - 1998    
     This postulates that 5-HT regulates the HPI axis.  This would be consistent with the  Direct Serotonin Pathway with some of the output of  Serotonin from the  Dorsal Raphe Nucleus going to the Anterior Pituitary . However, the data could just as easily be interpreted as indicating that the HPI axis regulates 5-HT, which would be consistent with the   Indirect Serotonin Pathway .   


Non-genomic Actions of Androgens   - 2008   
In toadfish, ... a territorial challenge it produces rapid elevations in calling behavior and circulating levels of the teleost-specific androgen 11-ketotestosterone (11kT).



THE REFERENCES

Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae).  - 1991   
http://www.ncbi.nlm.nih.gov/pubmed/2045087  
Only abstract available online.  I got the PDF through the library.   
    "Radioimmunoassay of plasma samples from individuals of known social status revealed that nonterritorial males have lower levels of Testosterone (T) and 11KT than territorial males.  Nonterritorial males allowed access to vacant territories underwent pronounced increases in T and 11KT." "... the endocrine system plays a role in fine-tuning the levels of territorial aggression exhibited by male stoplight parrotfish."


Effect of dominance status on sex hormone levels in laboratory and wild-spawning male trout.  - 1996  
http://www.ncbi.nlm.nih.gov/pubmed/8729943  
Only abstract available online.  I got the PDF through the library.   
    " In small groups of rainbow trout (Onchorhynchus mykiss) spawning in the laboratory,  Dominant males had higher plasma levels of Testosterone (T) and 17 alpha, 20 beta-dihydroxy-4-pregnen-3-one (17,20 beta-P) compared with subordinates.  
    Steroid levels increased in subordinate males that became dominant after dominant males were experimentally removed; higher steroid levels in dominant males appears to be a result rather than a cause of their social status." 
    " In free-ranging brown trout (Salmo trutta) sampled in the field, we found higher levels of 11-ketotestosterone (11KT) but not T in dominant males. No significant differences in levels of either androgen were found between dominant and subordinate male brook trout (Salvelinus fontinalis) sampled at the same field location."  "The different findings in the laboratory and field may ... reflect the relative uniformity of the laboratory environment; this simple environment may allow competitively superior males to more completely dominate less competitive tank-mates "


Serotonin as a regulator of hypothalamic-pituitary interrenal activity in teleost fish (PubMed)   - 1997   
http://www.imbv.uio.no/fys/groups/gorann/db04-publications/internet/html/docs/NSL230.pdf    
Full length PDF available online for free. 
    Since this is a long article, I've interspersed my comments throughout the text rather than providing them all at the end.   
    "It appears clear that brain Serotonin (5-hydroxytryptamine, 5- HT) synthesis and turnover is affected by  Stressful events. Further, there are results suggesting that the Sympathetic Nervous System (SNS) as well as the HPA Axis are involved in mediating stress-induced alterations in the 5-HT system of the mammalian brain."   
My comment #1
    This supports my view in 'Boys without Fathers' that the level of 5-HT is, in part, controlled by the HPA (cortisol) + testosterone axis.   See: Indirect Serotonin Pathway .
more from the reference:     
    "Reciprocally, the serotonergic system appears to be involved in the control the HPA axis and SNS in mammals. Thus, the brain 5-HT system could play a pivotal role in a complex neuroendocrine loop serving to defend homeostasis and promote acclimation during physiological or environmental challenges." 
My comment #2
    Feed back loops are quite common in both the nervous and the endocrine systems.  However, they are always negative feedback loops.
more from the reference:       
    "Still, the role of brain 5-HT in HPA axis regulation has been debated, especially since direct 5-HT innervation of the mammalian Paraventricular nucleus (PVN) , the crucial focus for central regulation of the HPA axis, is limited." 
My comment #3
    The fact that the 5-HT innervation of the paraventricular nucleus is 'limited' may indicate that this is the minor arm of the feedback loop and that the  Cortisol + Testosterone axis is the major arm.  They don't give any other explanation of how Serotonin (5-HT) influences the HPA Axis
more from the reference:     
    "The anatomical organization of the brain serotonergic systems is remarkably conserved among vertebrates, implicating that 5-HT functions might also have been conserved.
    ... In a number of teleost species as well as in mammals, social  subordination and other stressors, including handling and predator exposure, elevates brain 5-HT activity, as indicated by brain 5-hydroxyindoleacetic acid ( 5-HIAA ; the major 5-HT metabolite) concentrations and 5-HIAA/5-HT ratios. The effect of  Stress on central 5-HT activity has a rapid onset and shows no signs of habituation. 
    As suggested in mammals, this elevation of brain  5-HT activity could mediate the stress-induced behavioral inhibition (see: Learned Helplessness ) characterizing socially subordinate fish.  In fact, pharmacological stimulation of brain 5-HT activity inhibits spontaneous locomotor activity and exploratory behavior in Arctic charr (Salvelinus alpinus), whereas inhibition of 5-HT synthesis by p-chlorophenylalanine has the opposite effect.  
My comment #4:   
    All of this describes an adaptive mechanism where stress precedes and causes elevated 5-HT which in turn leads to behavioral inhibition which can have a self-protective function.  However, they haven't said what the initial response to an external stressor is.  Cortisol is normally cited as fulfilling that role.   
more from the reference:     
    "However, brain 5-HT could also play an important role in the regulation of the HPI axis (the fish equivalent of the HPA Axis ). Socially subordinate fish display elevated plasma cortisol levels, and increased interrenal cell sizes, suggesting a chronic activation of the HPI axis." 
    "In mammals, the stimulatory role of 5-HT on the HPA axis has been attributed to 5-HT1A and 5-HT2 receptors (see: Serotonin Receptors )." 
My comment #5
    The chronic activation of the HPI axis is probably just due to the chronic stress of being subordinate. 
more from the reference:     
    "The aim of the present study was to examine if 5-HT1A-like receptors are involved in HPI axis regulation in the rainbow trout." 
    "These results show that the specific 5-HT1A receptor Agonist ,  8-OH-DPAT, is a potent activator of the interrenal stress-response in the rainbow trout." 
My comment #6
    Their data certainly shows the injection of a 5-HT1A agonist causing an increase in circulating cortisol.  Therefore, for this to be a negative feedback loop, an increase in cortisol must cause a decrease in 5-HT at the 5-HT1A receptor. 
more from the reference:       
    "Furthermore, it appears well established that 5-HT stimulates Corticotropin-releasing hormone (CRH) release from the mammalian hypothalamus and that 5-HT1A is the dominant receptor in mediating this effect.
    ... there is a growing body of evidence suggesting that 5-HT also acts directly at the Pituitary Gland , stimulating the release of ACTH. These pituitary effects of 5-HT have been attributed to 5-HT1A and 5-HT2 receptor activation.  Moreover, 5-HT has been reported to potentiate the effect of other ACTH   secretogogues, such as Arginine Vasopressin (AVP), suggesting a possible amine-peptide interaction at the level of the pituitary." 
My comment #7:  
    As above, for this to be a negative feedback loop, increases in CRH, ACTH and AVP must cause a decrease in 5-HT at the 5-HT1A receptor.   
more from the reference:     
    "The pituitary pars distalis ( Anterior Pituitary ) in teleosts is unique among vertebrates in that it is directly innervated by neurosecretory fibers and lack the portal system of the median eminence. Indeed, the only way 5-HT originating from the central nervous system can reach the pituitary is through direct innervation. Such innervation has been detected in some teleost species but Frankenhuis van den Heuvel and Niwenhuys could not demonstrate any structural relationship between brain 5-HT neurons and the pituitary gland in rainbow trout."   
My comment #8
    This suggests that injecting a 5-HT1A agonist into the dorsal aorta may have flooded the pituitary in an unnatural way.   
more from the reference:     
    "In addition to Corticotropin-releasing hormone (CRH) several other Neuropeptides / Hormones are involved in the regulation of ACTH secretion from the teleost pituitary. For instance, arginine vasotocin (AVT), isotocin (IT) and urotensin I (UI) are all potent ACTH secretouges  AVT and IT are teleost homologs of mammalian  AVP and oxytocin, respectively, whereas UI is a member of the CRH family of peptides.  5-HT have been reported to stimulate the release of AVP and oxytocin in mammals but the role of 5-HT in the regulation of production and release of AVT and IT in teleost fish has not been studied."  
My comment #9
    Although not immediately relevant to the 5-HT - cortisol feedback loop, I thought this information about AVT, etc., was interesting. 
more from the reference:     
    "In conclusion, the results from the present study show that 8-OH-DPAT elevates plasma Cortisol in catheterized rainbow trout in a dose-dependent manner. The effect of 8-OHDPAT is most likely mediated by activation of 5-HT1A-like receptors, 8-OH-DPAT being a highly selective 5-HT1A receptor Agonist .  
    This conclusion is further supported by the fact that previous results clearly show that 5-HT1A-like receptors are present in the brain of salmonid fish. However, at the present time, we do not know at which level of the HPI axis 8-OH-DPAT exerts its effect."     
My comment #10:  
    As noted in comment #8, above, injecting a 5-HT1A agonist into the dorsal aorta may have flooded the pituitary in an unnatural way.   
 


Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout.  - 1998         Abstract http://ajpregu.physiology.org/cgi/reprint/274/3/R645   
    Full length HTML available online for free. 
from the HTML   
Note:  I've rearranged the order of the quotes, below. 
    "The brain Serotonin (5-HT) system is also believed to exert an inhibitory effect on sensory-motor reactivity to environmental stimuli,"     
    "... the 5-HT system of the mammalian brain also appears to be inhibitory to behavioral responsiveness.  Socially subordinate fish frequently display a pronounced behavioral inhibition, an effect that could be mediated by brain 5-HT and represent a passive coping strategy in subordinate animals, lowering the frequency of  Agonistic interactions  with  Dominant individuals and thus possibly reducing the stress in subordinates." 
    "The hypothalamic-pituitary-interrenal (HPI) axis [the teleost homologue of the mammalian hypothalamicpituitary-adrenal axis ( HPA Axis )] consists of a series of Hormonal pathways, the major components being Hypothalamic   Corticotropin-releasing hormone (CRH), Pituitary adrenocorticotropin ( ACTH ), and interrenal Cortisol . Corticosteroid release is stimulated by ACTH secretion from the pituitary (rostral pars distalis) ( Anterior Pituitary ), which in turn is regulated by CRH ( See: Abbreviations ).  
    ... ACTH and several other biologically active peptides , e.g., a-melanocyte-stimulating hormone (a-MSH), b-lipotropin, and the endogenous opioid b-endorphin, are all synthesized from a common precursor protein, pro-opiomelanocortin (POMC)." 
    " Agonistic Behavior , brain concentrations of Serotonin (5-hydroxytryptamine, 5-HT), and 5-hydroxyindoleacetic acid ( 5-HIAA , the main 5-HT metabolite), plasma Cortisol levels, and the Pituitary expression of pro-opiomelanocortin (POMC) A and B mRNA were determined in socially Dominant and subordinate rainbow trout after 1 or 7 days of social interaction. 
    Telencephalic and brain stem 5-HIAA/5-HT ratios, plasma cortisol levels, and pituitary POMC mRNA concentrations were elevated in fish being subordinate for 1 day.  Furthermore, neither telencephalic 5-HIAA/5-HT ratios nor pituitary POMCA or POMC B mRNA expression showed any decline after 7 days of social interaction. 
    By contrast, plasma  cortisol concentrations of subordinate fish declined after 7 days but were still significantly higher than in dominant fish.  Furthermore, in subordinate fish, hypothalamic 5-HIAA/5-HT ratios and plasma cortisol levels were highly correlated, suggesting an important role of hypothalamic 5-HT in the regulation of the teleost hypothalamic-pituitary-interrenal (HPI) axis." 
    "Treatment with 8-hydroxy-2(di-n-propylamino)tetralin, a specific 5-HT1A receptor (see: Serotonin ReceptorsAgonist , elevates plasma cortisol concentrations in catheterized rainbow trout in a dose dependent manner, and this strongly supports the view that 5-HT regulates the HPI axis."  
My comments
1.    This postulates that 5-HT regulates the HPI axis.  This would be consistent with the  Direct Serotonin Pathway with some of the output of  Serotonin from the  Dorsal Raphe Nucleus going to the Anterior Pituitary .     
2.   However, the data could just as easily be interpreted as indicating that the HPI axis regulates 5-HT, which would be consistent with the   Indirect Serotonin Pathway with a decrease in the HPI axis allowing  Testosterone to rise which in turn lowers 5-HT.  Or, the other way around, an increase in the HPI axis suppresses testosterone production by the testes which in turn allows 5-HT to rise.  
3.   This article is also analyzed in Cortisol & Dominance . One of the copies should just contain a link to the other page.


Non-genomic Actions of Androgens (PubMed)  - 2008
Full length HTML and PDF available online for free. 
    "Rapid actions of androgens on behavior are not confined to mammalian species. In toadfish, males call to attract females to their nesting sites. Field experiments have demonstrated that when males are faced with a territorial challenge it produces rapid elevations in calling behavior and circulating levels of the teleost-specific androgen 11-ketotestosterone (11kT)." 
    See also:  Androgens .    




Teleost Dominance Hierarchies
130129 - 0742
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