14 - Boys Without Fathers: An Endocrine Hypothesis

Cross references:  

CDEV 74


Lou Morgan


Term Paper

December 9, 2004




Boys Without Fathers:

An Endocrine Hypothesis




Overview:


Socially deviant adults often show abnormalities in their endocrine systems. The most commonly found abnormalities are decreased serotonin activity and increased levels of circulating testosterone, and when both testosterone and serotonin are measured, these abnormalities are found together. Adults showing this endocrine profile bear a variety of labels. The most common is "personality disorder", but others showing the same endocrine profile are variously labeled "criminal", "rapist", "fire setter", "violent offender" and "impulsively aggressive". People with this endocrine profile also have very high rates of both homicide and suicide. Statistical analysis of the variations among people with these abnormalities shows that the increased testosterone is responsible for the aggression common to the syndrome, while the reduced serotonin is responsible for the impulsiveness [1, 2].


A somewhat similar, but less clear-cut, endocrine profile is found among younger people who bear the labels "delinquent", "antisocial", "disruptive", "hyperactive" and "conduct disordered". [3, 4].


In none of the articles discussing people with the above endocrine profile was there any mention of the family structure in which the individuals having the profile had grown up. In particular, there was no way of telling whether or not they had grown up without a father. However, studies have shown that approximately 70% of the prison population is boys who have grown up without a father [5]. So there is probably considerable overlap between individuals having the above endocrine profile and men who

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have grown up without a father. This paper presents an hypothesis as to why a boy who grows up without a father might end up with the above endocrine profile and all of the difficulties that seem to come with it.


As you may already know, there is a phenomenon, usually referred to as the "male dominance hierarchy", which seems to be almost universal among all but the most primitive vertebrates [6]. I will argue that boys who grow up without the influence of an older, dominant male, such as a father, develop the endocrine profile discussed above because they have never received the training which would allow them to control their endocrine systems and that young men who do have fathers, or grow up under the influence of older, stronger males, receive this training as they work their way up the male dominance hierarchy.


The male dominance hierarchy has been studied mostly in its relationship to sexual reproduction and mostly as it relates to testosterone, the male sex hormone. However, it also involves estrogen, the female sex hormone, cortisol, sometimes thought of as the stress hormone, the neuropeptide arginine vasopressin, and the neurotransmitter serotonin.


Since both the nervous system and the endocrine system become increasingly complex during the course of evolution, this paper is organized in an evolutionary sequence, starting with the cephalocordate, amphioxus, and concluding with we humans. This means that, as we work our way up the evolutionary ladder, we will discuss the consequences of new physiological advancements as we come to them, even though these consequences have not yet been identified in the first organism in which they appear. In particular, rats, mice and hamsters are the most frequent laboratory subjects, but the specific physiological structure or relationship discussed in a report of an experiment using one of these rodents may have originally evolved in a more primitive predecessor. In order to highlight the behavioral consequences of the physiological structure or relationship under consideration, its consequences will be discussed at the evolutionary level where it first appears even though the understanding of these consequences was achieved through experiments with animals (usually rodents) that are more evolutionarily advanced.


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Amphioxus:


The amphioxus is a small (2 inch) fish-like creature that lives in shallow, somewhat warmer, coastal waters over a wide range. Its only well developed sensory modality is touch, but, though it has no real eyes or ears, it is aware of both light and sound. It may also have very rudimentary senses of taste and smell, but this is uncertain. Although it is denied membership among the vertebrates because it does not have an articulated backbone, it is widely seen as representing the final step leading to the vertebrates' eventual evolution [7].


What concerns us here is its endocrine system. It should be noted first that arginine vasopressin is found only in mammals. Its analogue in nonmammals is the very similar arginine vasotocin. With this proviso, there is evidence in the amphioxus for four of the five above mentioned bioactive compounds (testosterone, estrogen, cortisol, arginine vasotocin and serotonin), but only the sex hormones testosterone and estrogen and the neurotransmitter serotonin, are involved in the same behaviors that they mediate in humans.


In humans, the hypothalamus produces gonadotropin releasing hormone which is conveyed to the pituitary gland through the hypophysial portal circulation. In response, the anterior pituitary releases luteinizing hormone into the blood. In males, the luteinizing hormone causes the testes to produce testosterone, and in females it causes the ovaries to produce estrogen. The testosterone or estrogen are then released back into the blood [8].


Although the reproductive physiology of amphioxus is much more primitive than that of the mammals, it shows the same broad outlines. In particular, the levels of the sex hormones testosterone and estrogen are controlled by the release of luteinizing hormone from the amphioxus analog of the pituitary gland and peak during the breeding season [9].


Throughout the vertebrates, beginning with the amphioxus, serotonin inhibits behavioral responsiveness [10], and serotonin is found in the amphioxus brain in a position

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approximately analogous to its position in the brain of mammals [11]. Both testosterone and estrogen interfere with serotonin-induced behavioral inhibition by desensitizing serotonin receptors, and they thereby increase behavioral responsiveness [12].


The adult amphioxus spends its life in large colonies buried just beneath the surface of the sand. There is no indication of any arrangement by rank or gender. As the levels of testosterone and estrogen peak during the breeding season, they reduce serotonin-induced behavioral inhibition, and the animal becomes ready to spawn. The exact trigger for spawning has not yet been discovered, but when they do spawn, they leave the sand and swim to the surface. The males and females mingle together while releasing their sperm and eggs into the surrounding water. They then return to the sand. There is no indication of any competition among them or male dominance hierarchy [13].


This very simple mating ritual is paralleled by the primitive state of some of the bioactive compounds important in mammalian reproduction. Arginine vasotocin is only found in the amphioxus spinal cord, not the brain as with humans [14], and there is almost no evidence for the presence of cortisol.



Cyclostomes:


The next evolutionary stage above the amphioxus which has still living members, and the most primitive of the true vertebrates, are the cyclostomes. The two existent genera are the lamprey and the hagfish. Since hagfish live in salt water, usually at considerable depth, while lampreys always spend at least some of their life cycle in fresh water, much more is known about the lamprey. In addition, the lamprey and the hagfish parted company about 400 million years ago during the Devonian, when the lamprey swam inland to become our ancestor and the hagfish stayed in the sea. So the hagfish will not be considered here.


The brain of the lamprey is a quantum leap up from the brain of the amphioxus [15]. Unlike the amphioxus, which has neither eyes nor ears and only a very questionable ability to taste or smell, the lamprey has fully functional eyes and

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ears, and definite appreciation for both tastes and odors. In order to handle all this extra input, the lamprey brain has expanded enormously. Its endocrine system has also advanced over that of the amphioxus.


The major advancement at this evolutionary level, among the bioactive compounds we are considering, is that arginine vasotocin is now found in the same parts of the brain in which arginine vasopressin is found in mammals [16]. There is a complex three way interaction between testosterone, arginine vasotocin/vasopressin and serotonin.


The hypothalamus contains receptors for arginine vasotocin/vasopressin, and an increase in arginine vasotocin/vasopressin at these receptors increases aggression [17]. However, the number of receptors present depends on the testosterone level, so that increased testosterone levels increase the number of arginine vasotocin/vasopressin receptors and, therefore, the response to arginine vasotocin/vasopressin [18].


In addition, the hypothalamus also contains serotonin receptors, and serotonin at these receptors reduces the sensitivity of whatever arginine vasotocin/vasopressin receptors are present [19]. At the same time, however, as discussed in relation to the amphioxus, testosterone reduces the sensitivity of serotonin receptors and thereby helps maintain the ability of arginine vasotocin/vasopressin to initiate aggression.


Therefore, testosterone increases aggression by two mechanisms: increasing the number of arginine vasotocin/vasopressin receptors and interfering with the generalized inhibitory effect of serotonin. This reduction in the generalized inhibitory effect of serotonin also results in what is known in humans as "impulsivity".


In addition to their potential modulation of the aggression promoting effects of arginine vasotocin/vasopressin outlined above, testosterone, estrogen and serotonin continue to play their roles in reproduction as they had in amphioxus, and serotonin has extended its presence and effects throughout the newly enlarged lamprey brain in a pattern consistent

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with that found in mammals [20]. Only cortisol does not appear to have achieved the level of importance that it has in mammals. In fact, it is almost undetectable in lampreys. This is because the adrenal gland, which is the source of cortisol, has only just begun to evolve [21].


There is still no evidence of intraspecies aggression or a male dominance hierarchy [22]. River lampreys build nests which are used year after year. As many as thirty will gather together to spawn in a manner very reminiscent of the amphioxus [23].



Modern Fish


Although the adrenal gland of modern fish has still not evolved into the compact, well defined organ found in mammals [24], it has finally reached the point where it can produce significant levels of cortisol [25]. It is probably not a coincidence that it is also among the fish that we find the first evidence of a testosterone-associated male dominance hierarchy. I will give two examples.


Among rainbow trout spawning in a laboratory tank, the dominant males have higher testosterone levels than the subordinate males. When the dominant male is removed and a previously subordinate male becomes dominant, the newly dominant male undergoes a pronounced increase in testosterone level [26].


In free living parrotfish at Glover's Reef in Belize, dominant males have relatively higher testosterone levels and defend territories that include several females. Subordinate males have relatively lower testosterone levels and do not defend a territory. If a subordinate male is moved to a vacant territory, it becomes a dominant male, defends its territory and experiences a rise in its testosterone level [27].


Unfortunately, in both of the papers above, only the testosterone was measured. No mention is made of serotonin, arginine vasotocin or the newly evolved cortisol. However, we already know from our discussion of the amphioxus that testosterone increases behavioral responsiveness by

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interfering with serotonin's inhibitory effect. Therefore the decreased testosterone of the subordinates reduces their behavioral responsiveness by permitting serotonin to have its inhibitory effect.


Cortisol directly inhibits the testicular receptor for luteinizing hormone, and this, in turn, reduces the level of circulating testosterone [28, 29]. Therefore, it is easy to surmise that the low levels of circulating testosterone in subordinate males is due to increased levels of the newly evolved cortisol, but this inverse relationship was not directly observed in the above studies. It was, however, observed in the next study to be discussed.



Marsupials:


There is a fundamental difference between fish and mammals. Mammals have a cerebral cortex. Fish don't. Nevertheless, it is generally accepted that this addition of a cerebral cortex did not alter the already established relationships among the various elements of the endocrine system. This provides a justification for taking an observation made on the sugar glider, which is a marsupial, and using it to help explain the male dominance relationship found among fish.


A study of social status among sugar gliders showed that dominant males have lower cortisol levels and higher testosterone levels than subordinates. Furthermore, if a dominant male is transferred to another colony where he finds himself in a subordinate position, his cortisol level rises and his testosterone level falls [30]. This inverse relationship between cortisol and testosterone, with cortisol level being the cause and testosterone level being the effect, is thought to be consistent among all vertebrates above the lamprey and a central element of the male dominance hierarchy.


We now have the outlines of the endocrinology of the male dominance hierarchy. The loser in a contest between two males experiences an increase in cortisol levels consistent with a fear reaction as a consequence of losing. The increased cortisol reduces circulating testosterone. This,

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in turn, both reduces the number of arginine vasotocin/vasopressin receptors and unleashes the inhibitory influence of serotonin. As a result, the defeated male becomes submissive and nonaggressive.


But what is the evolutionary advantage of this? It forces the defeated male to seek a new, as yet unclaimed, territory for breeding, and this, in turn, promotes the dispersal and long term survival of the species.



Rodents


There are hundreds of studies linking testosterone to aggressiveness in rodents. In particular, elevating the animal's testosterone level over an extended period of time increases aggressiveness not only in males [31, 32] but also in females [33, 34], and lowering the testosterone level has just the opposite effect [35]. What is most important here is the clear conclusion that, at least in rodents in a laboratory setting, there is a definite cause and effect relationship between testosterone and aggression.


Surprisingly, I was not able to find one single experiment which combined testosterone injection with manipulation of serotonin levels. Most of the serotonin articles dealt with primates or humans, but there were two that found a correlation between decreased serotonin and increased impulsivity in rodents [36, 37]. Unfortunately, neither of these measured testosterone or cortisol levels.


Although there are no published reports on the effect that injected testosterone has on serotonin, arginine vasopressin and cortisol, what we have already learned allows us a reasonable guess. In both males and females, as testosterone goes up, serotonin responsiveness goes down and arginine vasopressin responsiveness goes up. The animal becomes more active and aggressive and therefore more likely to prevail in dominance encounters. This lowers the level of cortisol, the stress and fear hormone. In males, the lowered cortisol level promotes release of testosterone by the testes which then supplements the effects of the originally injected testosterone.



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This has consequences for the dominance hierarchy because the more aggressive animal becomes dominant and the less aggressive animal is relegated to the subordinate position. In fact, in rodents in the laboratory, testosterone has such a major influence on the dominant/subordinate relationship that subordinate males become dominant if their testosterone level is raised and dominant males become subordinate if their testosterone levels are lowered [35].



Primates


Although I cannot find a reference for it, it seems to be generally assumed that the endocrine systems of primates and humans is pretty much the same as the endocrine system of rodents and that the differences in behavior as one goes up the phylogenetic scale from rodents to primates to humans is due to changes in the nervous system and not to changes in the endocrine system. Even the changes in the nervous system and its relationship to the endocrine system are more a matter of degree than the addition of any new structures. The rodent cerebral cortex has representations for all the primary senses but only limited capacity for making associations between the various senses. The primate cerebral cortex has evolved large association areas which allow for integrating the input from all the senses. The major change which characterizes humans is the enlargement of the prefrontal cortex which helps us guide our behavior in response to the emotional needs mediated by our endocrine systems [38].


Unlike the literature on rodents, there were far fewer articles on primates, and almost all of them concerned animals living outside the laboratory in more-or-less "free range" conditions. The one report which described the consequences of artificially elevating a primate's testosterone levels by testosterone injections confirmed that, as was the case with rodents, administration of testosterone resulted in increased aggression [39].


Three interesting studies looked for behavioral correlates to the levels of testosterone and a serotonin metabolite (5-HIAA) in the cerebrospinal fluid of free-ranging monkeys. The first showed that elevated testosterone correlated with increased aggression, reduced serotonin correlated with

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increased impulsivity, and the combination correlated with extreme, impulsive aggression [40]. The second showed that the impulsive monkeys with low serotonin were more likely to achieve social dominance, at which time their serotonin and impulsivity would return to normal [41]. The third showed that monkeys with low serotonin and high impulsivity that did not achieve social dominance had a very high mortality rate [42]. So evidently the low serotonin, high impulsivity monkeys either achieve social dominance through fighting or die trying. Most studies on primate groups with stable social structures did not find a significant correlation between testosterone and dominance rank [43, 44].



Humans:


Unlike the situation in rodents and even primates, supplemental testosterone does not induce overt aggression in normal adult males [45], but may cause minor aggressive mood changes [46] and some covert aggression in response to provocation [47]. As discussed at the beginning of this paper, normal adult males have both lower testosterone levels and higher levels of serotonin activity than those deviant adults that society labels "personality disordered", or "criminal" or "impulsively aggressive". However, it has been found that, in competitive situations between normal males, the testosterone level of the winners rises while the testosterone level of the losers falls [39]. Among healthy, normal adolescent boys not receiving supplemental testosterone, boys with higher testosterone levels do not show more overt aggression but are more impatient and irritable and more likely to respond to provocations or threats [49].


Although there are no scientific experiments which shed light on this, it is easy to speculate that the diminished influence of testosterone on the behavior of normal humans, as compared to rodents and primates, is due to the moderating influence of our greatly expanded prefrontal cortex.



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The Hypothesis:


The outlines of my hypothesis are probably pretty clear by now. Boys who have fathers grow up thoroughly subordinate to their dominant fathers, and this is reflected in their endocrine systems. Domination by their fathers maintains their cortisol at high enough levels that their testosterone levels are held in check. This prevents the inappropriate proliferation of their arginine vasopressin receptors, which reduces their aggressiveness, and permits the inhibitory effect of their serotonin systems, which reduces their impulsiveness.


As boys with fathers grow into manhood, their inclination toward male impulsiveness and aggressiveness is guided by their fathers into socially acceptable channels, such as competition in sports or in business.


By contrast, boys who grow up without a father or some other dominant father figure are in danger of having endocrine systems which have not been guided into socially acceptable channels. They become the high testosterone, low serotonin deviants branded by society as "criminals" who are "personality disordered" and "impulsively aggressive".



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42. Higley JD, Mehlman PT, Higley SB, Fernald B, Vickers J, Lindell SG, Taub DM, Suomi SJ and Linnoila M. (1996). Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. Archives of General Psychiatry. Jun;53(6):537-43.


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