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However, as is the case in many vertebrates, dominant male anoles differ in many behavioral and physiological traits beyond aggression , , , any of which could be related to AVT changes in different nuclei. Furthermore, a slowly emerging, stable state difference in the brain following long term experience in a social status is a different characteristic than immediate activation during a specific behavior. Although much work remains to be done in order to understand the role of various AVT populations in social behavior and their modification as a consequence of that behavior, the results of these studies suggest a complex network of forebrain AVT cell populations participating in a variety of male social behaviors.

Louis J. Guillette Jr.

Few studies have taken the more direct approach by treating males with exogenous AVT. Dunham and Wilczynski did this using intraperitoneal injections of AVT in male green anoles. AVT injections decreased, rather than increased, aggressive displays to a mirror Figure 4.

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Although at first this may seem contrary to expectations, in fact AVT has been found to have opposite effects depending on species and context. Green anoles are territorial, and most consistently across species of birds and fish AVT tends to suppress aggressive behavior in territorial individuals, species, or morphs while stimulating it in non-territorial or socially gregarious animals 4 , AVT did not, however, influence aggression or the outcome when AVT treated male anoles interacted with size-matched saline injected males.

This is of course a more complicated situation where the interaction between the two males determines the level of behavior in each as well as the outcome of the encounter.

TOPIC 2 (part 1) : FISH REPRODUCTIVE PHYSIOLOGY (Fish Reproductive organ)

This dominant-subordinate difference may represent lower release of the aggression-suppressing peptide in the more aggressive dominants. Note that this is similar to the argument regarding AVT cell variation in male cricket frogs, that is, that the higher release of the call-stimulating peptide results in smaller sized and a lower number of AVT-containing cells in calling vs. Figure 4. From data in Dunham and Wilczynski Interestingly, AVT treatment of male anoles does not change the number of courtship displays to a novel female; however, females were significantly more responsive to AVT-injected males AVT must have modified some aspect of male courtship signaling, either through subtle changes in the form of the observable visual displays not yet documented, or through some modulation of signals not readily apparent such as pheromonal signals.

Chemical signaling is poorly understood in anoles but is present in many lizards AVT does influence responses to conspecific odors in male European Common Lizards Zootoca vivipara , where it suppresses attraction to odors of other conspecific males. Whether females are similarly affected by AVT is unknown. Social bonding, which is a function of nonapeptides in mammals 1 , is usually considered beyond the realm of reptiles, and in fact most lizards, turtles, and snakes do not pair-bond or show parental care.

Some viviparous snakes do, however, show mother—offspring brooding-like behavior and defense of their offspring.

It is worth noting that in addition to many species of snakes, skinks in the order Scincidae also show parental care, and crocodilians are virtually bird-like in their nesting behavior. This species diversity provides ample opportunities for extending the investigation of reptilian AVT into areas of social behavior beyond simple aggression and courtship responses, just as the expected diversity of frog social behavior beyond male advertisement calls and female responses does for amphibians.

In reptiles, AVT, like AVP in mammals, is a peripherally acting peptide hormone influencing osmoregulation, which in reptiles is also tied to thermoregulation, and stimulating smooth muscle contraction, including oviduct contractions associated with oviposition 55 , — Similarly, osmoregulation is an important peripheral function of amphibian AVT , Treatments with exogenous AVT stimulate water absorption in both anurans and urodeles ICV AVT injections also stimulate water absorption indicating that AVT also acts as a central nervous system modulator of hypothalamic centers regulating water retention.

Diakow and Nemiroff 48 in fact suggested that the AVT triggered decrease in female release calling was due to water absorption, leading to abdominal extension mimicking a large egg mass. This may have contributed to her experimental results, but it is not at all clear how this would account for the enhancing effects of AVT on release calling in males. Particularly important in the context of its effects on social behavior, AVT is a potent stimulator of adrenal gland steroid hormone secretion in both amphibians Figure 5 and reptiles 68 , , , just as AVP is in mammals.

High cortisol levels can dramatically change social behavior in many vertebrates by various mechanisms including interaction with other hormones and, although less well studied, possibly through glucocorticoid effects on glucose metabolism and related energetic functions. Although peripheral AVT action is less a concern in studies investigating natural variation of brain AVT measures with behavior, those peripheral effects are problematic for experiments employing systemic treatment with exogenous AVT or vasopressin receptor blockers, as these procedures will influence bodily physiological functions in addition to, and perhaps more than, AVT signaling in the brain.

On the other hand, the fact that AVT treatment in frogs increases calling rates even though it also increases corticosteroids 68 Figure 5 suggests that AVT positively influences calling independent of, and in spite of, any negative effects of elevated corticosteroids.

Hormones and Reproduction in Fishes, Amphibians, and Reptiles

Figure 5. Results show that AVT increases calling even when stimulating corticosteroid release. From data in Burmeister et al. AVT-containing cells, consisting of both magnocellular and parvocellular neurons, are found mainly in limbic forebrain and hypothalamic areas with a widespread fiber distribution throughout the central nervous system marked by a particularly heavy innervation of the limbic Social Decision Network and associated social communication areas of the brain. There is generally a male-biased sexual dimorphism in the anatomy, although with several reported exceptions.

Finally, AVT has both peripheral physiological effects common across vertebrates and modulatory influences on social behavior and communication. These behavioral effects are most consistently observed in males, but are now seen as modulating female social behavior as well in the few cases where it has been investigated. There is evidence that AVT modifies chemical, visual, and auditory processing in urodeles and anurans 39 , 63 , channels used in various species for their communication. There is also direct physiological evidence as well as suggestive neuroanatomical data that implicate action on motor areas Of course, it is possible that AVT acts in multiple, and perhaps independent, ways, both centrally and peripherally, or that AVT in some way acts to bind these areas together by modifying a functional network linking them.

An important step toward understanding exactly what this peptide is doing would be formulating truly testable hypotheses explaining the mechanisms by which changes in peptide levels result in changes in specific aspects of social behavior. The diversity seen in the AVT system represents both a challenge to understanding its mechanism of action and a potential tool to investigate it.

Although the widespread fiber distribution is common across species, species variation in the location of AVT cells themselves is apparent in Table 1. This diversity needs to be viewed cautiously, as reports of AVT cell location in urodeles, anurans, and reptiles, go back over 30 years, and systematic, well controlled comparative studies remain to be done with modern methods. Nevertheless, if variation in the anatomical distribution of AVT neurons is real, an analysis of whether or not this is functionally relevant could make an important contribution to understanding the structure-function relationship of AVT and other neuroactive peptides.

The AVT system is a dynamic one, sensitive to multiple factors within and across individuals. In addition to a consistent sex difference within species, AVT characteristics vary within individuals based on seasonal, social, and hormonal state. The influence of steroid hormones on AVT levels and possibly action is particularly profound. The influence of melatonin on AVT neurons shown in anurans 16 is also an aspect that deserves further explorations in the other groups.

Whereas AVT consistently influences social communication and aggression across species, what is influenced and how it is modulated can vary greatly. For example, AVT influences chemical signaling in urodeles, vocal signaling in anurans, and visual displays in reptiles; in the first two taxa, AVT increases the propensity to signal, whereas in reptiles, at least in an aggressive context, it decreases visual signaling spontaneous display behavior has not been assessed in lizards. Moreover, all possible effects of AVT on male frog aggressive calling have been reported: decreased aggressiveness 65 , increased aggressiveness 70 and no effect How the link between AVT function and behavioral output can vary so dramatically remains an important gap in our knowledge.

Although a challenging issue, the species diversity across urodeles, anurans, and reptiles in social behavior also represents an opportunity to dissect the way in which AVT acts on the neural systems responsible for social behavior. Anuran species, for example, range in calling sex dimorphism from vocal advertisement signaling being strictly a male behavior, to females producing audible calls other than advertisement calls, to both males and females producing advertisement calls.

Visual displays are an important adjunct to vocal signals in some anuran species, but not others. Release signals produced by both males and females have both audible and vibratory components in some species, but only vibratory in others. How is this diversity within and between sexes reflected in either the anatomical or physiological characteristics of brain AVT? Extending the type of structure-function analysis used to implicate AVT function within species to the diversity seen among species could provide real insight into how social peptides evolve and operate. All authors discussed and planned the paper.

All authors reviewed and edited all sections of the paper, which was then compiled by the corresponding author. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Oxytocin, vasopressin, and the neurogenetics of sociality. Science —4. Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors.

Horm Behav 36 1 — The emergence of the vasopressin and oxytocin hormone receptor gene family lineage: clues from the characterization of vasotocin receptors in the sea lamprey Petromyzon marinus. Gen Comp Endocrinol — Brain Res Brain Res Rev 35 3 — Goodson JL. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48 1 — Distribution of vasotocin- and mesotocin-like immunoreactivities in the brain of the South African clawed frog Xenopus laevis.


J Chem Neuroanat 5 6 — Neuroanatomical distribution of vasotocin in a urodele amphibian Taricha granulosa revealed by immunohistochemical and in situ hybridization techniques. J Comp Neurol 1 — Neuroanatomical distribution of vasotocin and mesotocin in two urodele amphibians Plethodon shermani and Taricha granulosa based on in situ hybridization histochemistry. Brain Res 1 :1— Vandesande F, Dierickx K.

Immunocytochemical demonstration of separate vasotocinergic and mesotocinergic neurons in the amphibian hypothalamic magnocellular neurosecretory system. Cell Tissue Res 3 — Jokura Y, Urano A.

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An immunohistochemical study of seasonal changes in luteinizing hormone-releasing hormone and vasotocin in the forebrain and the neurohypophysis of the toad, Bufo japonicus. Gen Comp Endocrinol 59 2 — Projections of luteinizing hormone-releasing hormone and vasotocin fibers to the anterior part of the preoptic nucleus in the toad, Bufo japonicus. Gen Comp Endocrinol 60 3 —7. Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. JComp Neurol 1 — Sexual dimorphism in the vasotocin system of the bullfrog Rana catesbeiana.

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  7. JComp Neurol 2 — Forebrain arginine vasotocin correlates of alternative mating strategies in cricket frogs. Changes in plasma testosterone levels and brain AVT cell number during the breeding season in the green treefrog. Brain Behav Evol 75 4 — Lutterschmidt DI, Wilczynski W. Sexually dimorphic effects of melatonin on brain arginine vasotocin immunoreactivity in green treefrogs Hyla cinerea.

    Brain Behav Evol 80 3 — The effects of melatonin on brain arginine vasotocin: relationship with sex and seasonal differences in melatonin receptor type 1 in green treefrogs Hyla cinerea. J Neuroendocrinol 27 8 —9. Bons N. Immunocytochemical identification of the mesotocin- and vasotocin-producing systems in the brain of temperate and desert lizard species and their modifications by cold exposure.