Mammalian nonapeptides activate territorial behavior in an amphibian
Introduction
Nonapeptides are an archaic family of conserved peptides that have evolved for > 700 million years. Functional properties of nonapeptides and their phylogenetic dispersion within vertebrate clades are wide-ranging and diverse [1], and yet the biochemical differences among the nonapeptides are remarkably minor [2]. Vasopressin- and oxytocin-related nonapeptides are present in representatives of both protostomian and deuterostomian lineages [3], [4], [5], [6], [7], [8]. This suggests that this signaling system originated very early in metazoan evolution. Due to the structural and positional similarities of the vasopressin and oxytocin genes it is hypothesized that they originated from the duplication of a common ancestral gene, likely following the radiation of the jawless fish about 500 million years ago [3], [6], [9], [10]. This genetic event is certainly plausible since gene duplication is a common evolutionary pathway toward the adaptation of genes to new functions [11].
Arginine vasopressin (VP) and oxytocin (OT) are two nonapeptides that are present in mammals and execute a wide array of physiological and behavioral functions [12]. In other classes of vertebrates these two neuropeptide systems are not present but homologous neuropeptide systems are existent. Instead of VP, arginine vasotocin (VT) occurs in birds, reptiles, amphibians, and fish [2], [3]. Co-evolving with these peptides were their respective receptors and signaling pathways that are responsible for conducting molecular and cellular functions.
Functionally, nonapeptides execute an assortment of physiological and behavioral tasks. Traditionally, VP is known as an antidiuretic hormone for its role in water retention [13], vasoconstriction [14], and water homeostasis [15]. Meanwhile OT is classically recognized for its physiological role during parturition and lactation [16], [17], [18]. Intriguingly, a large volume of literature has been generated on the behavioral outcomes of nonapeptides. While substantial variation ensues between taxa, all linages of vertebrates are characterized by having specific behaviors governed by these peptides that can include: aggression, agonistic behavior, pair-bond formation, vocalizations, gregariousness, cooperation, and paternal and/or maternal care [for reviews see: [1], [3], [19], [20], [21], [22]].
A number of investigations (and reviews) on nonapeptides have concentrated on the functional aspects of nonapeptide systems [23], [24], [25], [26], [27]. While the majority of these studies have utilized mammals as their model organism some have employed amphibians [28], [29] and fish [30], [31]. For example, it was discovered replacing the fish gene for isotocin (teleost homolog of OT) with the mammalian gene for OT in transgenic rats did not adversely affect their physiology [31]. Further, it was demonstrated that the mammalian nonapeptides, OT and VP, can modulate social behavior in fish [32]. This could indicate that receptor mechanisms and signaling factors mediating the physiological regulation of nonapeptides are possibly conserved between mammals and fish. Investigations in both newts and frogs disclosed that both mesotocin and vasotocin 1a nonapeptide receptors are present [24], [28], [29]. In amphibians, the VT system activates indispensable social and reproductive behaviors [33], [34], [35], [36], [37] and it is firmly established that in male frogs VT activates territorial and reproductive behaviors [38]. In fact, previous research in the Puerto Rican coquí frog, Eleutherodactylus coqui, has demonstrated that VT will activate advertisement vocalizations [37]. These are signals used in the establishment and maintenance of territories as well as the attraction of mates. This investigation also found that exogenously activated, non-territorial frogs moved into and established new territories and commenced advertisement calling [39].
Clearly, nonapeptides perform a key role in the expression of social behaviors and that distinctive classes of nonapeptides exist in different clades of vertebrates. The objectives of this investigation were to 1) determine if the closely related non-amphibian nonapeptides, VP and OT, would activate territorial behavior in male Puerto Rican coquí frogs, E. coqui; 2) determine if non-territorial frogs move into new territories and commence advertisement calling, and 3) to elucidate, if VP and/or OT activate additional and/or alternative social or reproductive behaviors. Due to functional and structural components of nonapeptide receptor-ligand binding properties it is hypothesized that VP and OT will activate advertisement calling and territorial behaviors in E. coqui.
Section snippets
Field site locations
Field work was carried out at two locations: 1) the Caribbean National Forest located in the Luquillo Mountains of northeastern Puerto Rico, approximately 1 km east of the El Verde Field Station (350–400 m) of the University of Puerto Rico at Rio Piedras; and 2) the Waiakea Field Research Area (500 m) of the University of Hawai‘i at Hilo, 924 Stainback Rd., Hilo, HI. Permits were obtained from the Departmento de Recursos Naturales y Ambientales of Puerto Rico and from the Department of Land and
Advertisement call activation
Activation of advertisement calling was significantly higher in VP-injected silent males (33/50) compared to saline-injected silent males (0/50) (p < 0.00001, Fisher's Exact Test) (Table 1; Fig. 1). VP-injected territorial males (42/50) were not significantly more activated to call than saline-injected territorial males (37/50) (p = 0.326, Fisher's Exact Test) but did have significantly higher call activation than saline-injected silent males (0/50) (p < 0.00001, Fisher's Exact Test). There was not a
Discussion
Results indicate that the mammalian nonapeptides VP and OT significantly activated advertisement calling and territorial behavior in the anuran amphibian, E. coqui. Further, the VP- and OT-injected males were as significantly activated to emit advertisement frogs as VT activated males. Interestingly, a major difference between exogenously activated males was that silent males relocated into a new area prior to initiating advertisement calling significantly more often than territorial males in
Conclusions
The mammalian neuropeptides VP and OT significantly activated advertisement calling and territorial behavior in male E. coqui. This activation was as robust as activation accomplished with the amphibian nonapeptide VT. Interestingly, nonapeptide activation also affected males differently. Following exogenous injections of VP and OT territorial males remained in their current territory but silent males moved into new areas and only then began to emit advertisement calls; this difference in male
Acknowledgments
We are grateful to the Departmento de Recursos Naturales y Ambientales of Puerto Rico for issuing collecting permits to work on E. coqui. Very special thanks goes to the staff at the El Verde Field Station (EVFS), Puerto Rico for providing support and use of their facilities, especially to Dr. Alonso Ramírez (Director of EVFS), Dr. Jill Thompson, and Ms. Hilda Lugo. The field station is part of the Long-Term Ecological Research project of the Institute for Tropical Ecosystem Studies, University
References (58)
- et al.
Evolution of vertebrate neuropeptides
Brain Res. Bull.
(2001) Neuropeptide families and their receptors: evolutionary perspectives
Brain Res.
(1999)- et al.
Molecular evolution of the oxytocin-oxytocin receptor system in eutherians
Mol. Phylogenet. Evol.
(2013) Evolution by gene duplication: an update
Trends Ecol. Evol.
(2003)- et al.
Neuropeptides and the evolution of social behavior
Curr. Opin. Neurobiol.
(2000) - et al.
Physiology and pathophysiology of the vasopressinergic system
Best Pract. Res. Clin. Anaesthesiol.
(2008) Vasopressin receptors
Trends Endocrinol. Met.
(2000)- et al.
Effect of cervical dilatation upon uterine contractility in pregnant women and its relation to oxytocin secretion
Am. J. Obstet. Gynecol.
(1964) Deconstruction sociality, social evolution and relevant nonapeptide functions
Psychoneuroendocrinology
(2013)- et al.
Social functions of individual vasopresson-oxytocin cell groups in vertebrates: what do we really know?
Front. Neuroendocrinol.
(2014)
Roles of arginine vasotocin receptors in the brain and pituitary of submammalian vertebrates
Int. Rev. Cell Mol. Biol.
Identification and characterization of mesotocin and V1a-like vasotocin receptors in a urodele amphibian, Taricha granulosa
Gen. Comp. Endocrinol.
Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs
Horm. Behav.
The neuropeptide arginine vasotocin alters male call characteristics involved in social interactions in the grey treefrog, Hyla versicolor
Anim. Behav.
Arginine vasotocin induces sexual behavior of newts by acting on cells in the brain
Peptides
Arginine vasotocin activates aggressive calls during paternal care in the Puerto Rican coquí frog, Eleutherodactylus coqui
Neurosci. Lett.
Arginine vasotocin activates advertisement calling and movement in the territorial Puerto Rican frog, Eleutherodactylus coqui
Horm. Behav.
Male parental care and its adaptive significance in a neotropical frog
Anim. Behav.
Serotonin modulates vocalizations and territorial behavior in an amphibian
Behav. Brain Res.
An enzymatically stable peptide with activity in the central nervous system: its penetration through the blood-CSF barrier
Brain Res.
Involvement of arginine vasotocin in reproductive events in the male newt Cynops pyrrhogaster
Horm. Behav.
The social behaviour of anuran amphibians
Anim. Behav.
Arginine vasotocin injection increases probability of calling in cricket frogs, but causes call changes characteristic of less aggressive males
Horm. Behav.
Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor
Horm. Behav.
Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs
Horm. Behav.
Treatment with arginine vasotocin alters mating calls and decreases call attractiveness in male túngara frogs
Gen. Comp. Endocrinol.
Arginine vasotocin increases calling-site acquisition by nonresident male grey treefrogs
Anim. Behav.
The effects of arginine vasotocin on the calling behavior of male cricket frogs in changing social contexts
Horm. Behav.
Historical perspective: hormonal regulation of behaviors in amphibians
Horm. Behav.
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Serotonin and vasotocin function in territoriality
2020, Pharmacology Biochemistry and BehaviorCitation Excerpt :Call latency did not include those data upon which a 5HT agonist inhibited calling all together. Variance in call latency was also observed in E. coqui when given exogenous (IP) injections of other nonapeptides (Ten Eyck, 2005; Ten Eyck and Ten Eyck, 2017) and may be a consequence of an IP injection in general. While extensive research on AVT in anurans has revealed multiple functions on advertisement calling, changes in calling behavior and characteristics, and promoting vocalizations with a varied spectrum (Boyd, 1994; Chu et al., 1998; Kime et al., 2010; Marler et al., 1995; Semsar et al., 1998; Ten Eyck, 2005).
Epigenetics of Social Behaviour
2019, Trends in Ecology and EvolutionCitation Excerpt :In rhesus macaque monkeys (Macaca mulatta), increased arginine vasopressin and oxytocin weaken the social hierarchy and increase behavioural synchrony between individuals [81]. It is likely that these behavioural responses are associated with increased group cohesion and decreased dispersal, and there is evidence that nonapeptides affect dispersal in an amphibian [82]. In a metapopulation, diversity among populations is beneficial because it renders the metapopulation more resilient to environmental change and perturbations [83].