Hormones and Animal Communication
Summary and Keywords
Animals produce communication signals to attract mates and deter rivals during their breeding season. The coincidence in timing results from the modulation of signaling behavior and neural activity by sex steroid hormones associated with reproduction. Adrenal steroids can influence signaling for aggressive interactions outside the breeding season. Androgenic and estrogenic hormones act on brain circuits that regulate the motivation to produce and respond to signals, the motor production of signals, and the sensory perception of signals. Signal perception, in turn, can stimulate gonadal development.
Many animals produce communication signals in different sensory modalities to attract mates, to coordinate gonadal development within mated pairs, and to deter rivals of the same sex. These signals are produced most often, or only, during the period of active breeding, and the coincidence in timing is a result of the modulation of signaling behavior and physiology by sex steroid hormones associated with reproduction. Circulating levels of androgenic and/or estrogenic hormones, and local estrogen synthesis in the brain, increase at the onset of breeding and stimulate different regions of the brain to increase signaling behavior. Steroids modulate signaling by acting on different brain circuits that regulate (a) the motivation to produce and respond behaviorally to signals; (b) the motor production of the signal; and (c) the sensory perception of the signal. The steroid sensitivity of these brain pathways provides a mechanism for coordinating communication behavior with reproduction. Signaling can be costly for the sender in several ways, including the energetic demands of neural and muscular activity required for signal production, decreased time for other behaviors such as foraging, and increased risk of exposure to predators and parasites. These costs are amplified because individuals may signal hundreds to thousands of times per day early in the breeding season. Steroid regulation of communication decreases these costs by restricting signaling to times of the year when it is required for breeding. Another benefit of steroid regulation is to provide a mechanism for sexually dimorphic development of brain regions required for signal production and endocrine responses to signals. In some taxa (fish, frogs), breeding signals are produced only by males, but females also signal in some reptilian taxa (e.g., Sceloporus lizards; Martins, 1991, 1993), some primate species (Geissmann & Orgeldinger, 2000; Pradhan, Engelhardt, van Schaik, & Maestripieri, 2006), and many species of birds (Odom, Hall, Riebel, Omland, & Langmore, 2014).
The relationship between signaling and steroid hormones has been studied most extensively for acoustic communication systems in ray-finned fish (Actinopterygii), frogs (anuran amphibians), and songbirds (oscine Passeriformes). Hormone modulation of electrocommunication in weakly electric fish (Mormyridae and Gymnotiformes) has also been studied in detail and shows many parallels to acoustic systems (Smith, 2013; Zakon, 1998, 2003). Steroid hormone modulation of visual displays has been shown in lizards (e.g., Sceloporus graciosus; Ruiz, French, Demas, & Martins, 2010), birds (e.g., golden-collared manakins, Manacus vitellinus; Fuxjager, Miles, & Schlinger, 2018), and perhaps also fish (Oliveira & Goncalves, 2008). Sex steroids and their metabolites excreted or secreted serve as chemical signals in many fish, amphibian, and mammalian taxa (Doyle & Meeks, 2018). Peptide hormones released by cells in the preoptic area of the brain (in fish and frogs) or anterior hypothalamus (in birds and mammals) may also modulate communication (Arch & Narins, 2009; Dunham & Wilczynski, 2014; Goodson & Bass, 2001; Grozhik et al., 2013). Neuromodulatory peptides include vasoactive intestinal polypeptide (VIP), arginine-vasopressin (AVP, mammals), arginine-vasotocin (AVT, fish, frogs, birds), oxytocin (OT, mammals), and isotocin (IT; the non-mammalian homolog of oxytocin). Given space constraints, only acoustic systems in vertebrates will be discussed in detail.
Steroid Modulation of Signal Production
Hormones act at multiple levels of the brain and periphery to modulate signaling behavior (Arnold, 1990; Ball, Riters, & Balthazart, 2002; Forlano, Schlinger, & Bass, 2006). Sex steroids act both on brain regions that control the motivation to signal (preoptic area, anterior hypothalamus), and on brain regions and muscles involved in the motor production of signals. This discussion of hormonal modulation of signal production will focus on birdsong as it is well studied and a learned behavior, unlike acoustic signals in most other vertebrates. It should be understood, however, that there are many similarities in the hormonal modulation of acoustic signal behavior and its underlying neuromuscular substrates in fish, frogs, and birds (reviewed in Forlano, Maruska, Sisneros, & Bass, 2016; Leary, 2009).
Sex Steroids Activate Song Behavior in Adult Birds
Song is produced at the highest rate during periods of intense reproductive activity when circulating blood concentrations of gonadal sex steroids, especially testosterone (T), are elevated. In males, T levels generally rise at the onset of the breeding season, fluctuate with different reproductive activities (e.g., courtship, nest building, incubating eggs, feeding young), and then decline to basal levels as breeding ends (Wingfield & Moore, 1987). Castration of males decreases or eliminates singing, and T treatment of castrated or intact males can increase song production (reviewed in Schlinger & Brenowitz, 2017). In some species (e.g., Island Canaries, Serinus canarius) adult females can be stimulated to sing by treatments with T. Other sex steroids, including 5α-dihyrdrotestosterone (DHT), 17β-estradiol (E2), and progesterone, are also elevated in the blood and/or brain of breeding male birds, and may contribute to song activation (Wingfield, Whaling, & Marler, 1994). In some species, song is also produced outside the breeding season, when circulating hormone levels are basal. Song may be used by nonbreeding birds to defend territories (e.g., Song Sparrow, Melospiza melodia; Smith, Brenowitz, Beecher, & Wingfield, 1997) or to maintain social cohesion in flocks and roosts (e.g., Red-winged Blackbird, Agelaius phoeniceus; Brenowitz, 1981). When produced outside the breeding season, song is given much less often, and with less stereotyped structure, than in breeding birds (Smith et al., 1997; Smith, Brenowitz, Wingfield, & Baptista, 1995). Activation of song in an aggressive context in nonbreeding birds appears to be regulated by the secretion of dehydroepiandrosterone (DHEA) from the adrenal glands, which is converted locally in the brain to T and E2 (Soma, Wissman, Brenowitz, & Wingfield, 2002). DHEA is an inert steroid precursor that does not stimulate hypertrophy of the reproductive system, with the associated energetic costs, in nonbreeding birds (Jalabert, Munley, Demas, & Soma, 2018).
Steroids Act on Neural Circuits That Regulate Signaling Behavior
The motivation to sing, the motor production of song, and song learning in birds are regulated by discrete neural circuits (Figure 1). Neurons at all levels of these circuits have receptors for androgen receptors (AR) and/or estrogen receptors (ER), and respond to steroid binding with changes in electrical activity and/or patterns of gene expression. The pronounced effect of sex steroids on these circuits is consistent with the close relationship between song behavior and reproduction.
Bass, Gilland, and Baker (2008) have noted that there is a striking evolutionary conservation of the overall organization of the vocal neural circuitry at the level of the caudal hindbrain and rostral spinal cord in acoustically signaling fish, amphibians, and birds. They suggest that the similarities in this circuitry across taxa arise from an ancestral, shared developmental origin in rhombomere 8. All of these vertebrate taxa have steroid receptors in neurons of midbrain and hindbrain structures involved in signaling. Unique among vertebrates, however, songbirds elaborated upon this ancestral circuitry by evolving a network of steroid-sensitive nonlimbic forebrain nuclei that have descending input to the hindbrain vocal circuit, and this may have been the definitive event in the evolutionary origin of the songbird (i.e., Oscine) lineage of Passerines (Brenowitz, 1997). Mammals evolved descending input from the motor cortex to the hindbrain vocal circuit (Jürgens, 2009), but differ from songbirds in lacking pronounced hormone sensitivity in the forebrain vocal regions.
Steroid Action on Neural Circuit for Motivation to Signal
The motivation to sing is mediated in reproductive birds by steroid activation of the medial preoptic area (POM) and midbrain central grey-intercollicular complex (CG/ICo) (Ball et al., 2002). CG/ICo projects to the sensorimotor song nucleus HVC (see Figure 1). Neurons in POM contain AR, and both AR and ER are present in CG/ICo neurons. T implanted in the POM of castrated male canaries increased the motivation to sing (Alward, Cornil, Balthazart, & Ball, 2018). Lesions of POM disrupted song production in male European Starlings (Riters & Ball, 1999), and electrical stimulation of CG/ICo evokes vocalization in several species (reviewed in Kingsbury, Kelly, Schrock, & Goodson, 2011).
Steroid Action on Neural Circuit and Muscles for Signal Production
The motor pathway controls the production of song. This circuit consists of projections from the thalamic nucleus Uva and the nidopallial nucleus NIf to HVC (not shown in Figure 1). HVC projects to the robust nucleus of the arcopallium (RA), and RA projects to the dorsomedial part of CG/ICo, the tracheosyringeal part of the hypoglossal motor nucleus in the brainstem (nXIIts) (Figure 1), and to respiratory control nuclei in the brainstem (not shown). Motor neurons in nXIIts send their axons to the muscles of the sound-producing organ, the syrinx. When these motorneurons are stimulated, the syringeal muscles contract and move two labial membranes into the expiratory air stream, which sets them into vibration to produce sound. Contraction of the syringeal muscles also changes the shape and/or length of the vocal tract, which influences the frequency composition of sounds produced by the labia (Suthers & Zollinger, 2004). The projection from RA onto the motor neurons in nXIIts is myotopically organized (Vicario, 1991). Neuronal activity in the premotor nuclei HVC and RA is synchronized with the production of sound by the syrinx (Fee, Kozhevnikov, & Hahnloser, 2004). If nuclei in the motor pathway are inactivated, a bird may adopt appropriate posture and beak movements, but does not produce sound (Nottebohm, Stokes, & Leonard, 1976).
AR are expressed at high levels in HVC, RA, NIf, ICo, nXIIts, and the syringeal muscles (Figure 1). HVC and ICo neurons also express ER. The RA-projecting neurons in HVC express only AR (Johnson & Bottjer, 1993; Sohrabji, Nordeen, & Nordeen, 1989).
Steroid binding by neurons in motor pathway can alter their electrical excitability and/or patterns of gene expression. The neurotransmitters norepinephrine (NE) and dopamine (DA), and tyrosine hdroxylase, the rate-limiting enzyme in catecholamine (CA) synthesis, are all present in HVC and RA, as well as area X and LMAN in the song learning circuit (see Steroid Action on Neural Circuit for Song Learning and Plasticity, and also Barclay & Harding, 1988). Castration of male Zebra Finches (Taenopygia guttatus) decreased NE and DA levels and turnover in RA, and E2 restored CA function (Barclay & Harding, 1990). Seasonal changes in circulating T levels alter the expression of genes in HVC and RA that are functionally related to neuronal birth and death, neuronal plasticity, neuronal excitability, angiogenesis, endocrinology, metabolism, and growth factors (Thompson et al., 2012).
Androgen has trophic effects on muscles involved in sound production. Muscle mass, cross-sectional fiber area, motor neuron endplate size, and/or twitch duration and speed increase in response to androgens in muscles involved in sound production in frogs (Girgenrath & Marsh, 2003), fish (Connaughton & Taylor, 1995), and birds (Bleisch, Luine, & Nottebohm, 1984). (Androgens also have trophic effects on muscles involved in visual signaling in frogs (Mangiamele & Fuxjager, 2018), lizards (Johnson, Kircher, & Castro, 2018), and birds (Fuxjager et al., 2018).)
Sex Steroids Influence Song Learning
Song in the oscine Passeriformes is distinctive because it is a learned behavior. In most, but not all, songbird species studied, if a young bird is raised in isolation from other birds, or deafened, it will never produce a normal song as an adult (Konishi, 1965; Marler, 1970; Thorpe, 1958). In many species a bird must hear song during a sensitive period in the first year of life to learn it (e.g., Zebra Finch). In other species, the sensitive period for learning opens again seasonally in adult birds (e.g., European Starling, Sturnus vulgaris; Beecher & Brenowitz, 2005; Brenowitz & Beecher, 2005). During the initial, sensory, phase of juvenile song learning, birds form a sensory memory or template of song that they hear conspecific adults produce. In the subsequent motor phase of learning, birds start to translate this sensory template into a motor program. Initially, a young bird emits sounds that bear only a slight resemblance to the memorized adult song. This first phase of subsong is marked by the production of crude sounds that are highly variable in structure. The young bird gradually improves its vocal performance during the next few months. By comparing auditory feedback of its own vocalizations to the memorized template, a bird comes to produce more polished sounds that increasingly resemble the template. This period of plastic song is characterized by variability in the order in which song syllables are combined. The bird continues to improve its performance so that when it becomes sexually mature at the onset of its first breeding season, it produces a crystallized song that has a well-defined stereotyped structure.
Sex steroids are important for song learning, signaling the onset and termination of sensitive periods for learning. Estrogens and androgens may have opposing functions that may open (estrogen), and close (androgen) sensitive periods of plasticity for new song learning (Bottjer & Johnson, 1997). E2 circulates at high levels in the blood of juvenile Song Sparrows and Swamp Sparrows (Melospiza georgiana; Marler, Peters, Ball, Dufty, & Wingfield, 1988; Marler, Peters, & Wingfield, 1987), when males are acquiring new song memories. E2 levels subsequently decrease when the birds begin to vocalize as young adults. Blood levels of E2 correlate with the degree of song learned by individual Swamp Sparrows (Marler et al., 1987).
Androgens are responsible for terminating the period of song plasticity so that the young adult bird produces a stereotyped version of conspecific song in its first breeding season. Birds castrated or treated with androgen antagonists at different stages of song learning are able to memorize a sensory template of adult song, and proceed through the early motor phases of song learning. On the one hand, without T, birds are unable to develop a stereotyped, complete version of conspecific song (Arnold, 1975; Bottjer & Hewer, 1992; Kroodsma, 1986; Marler et al., 1988). Implanting young birds with exogenous T, on the other hand, produces rapid crystallization, even of incompletely developed song (Korsia & Bottjer, 1991; Whaling, Nelson, & Marler, 1995). These studies show that exposure to high plasma levels of T at puberty is necessary for the production of a stereotyped version of conspecific song.
Steroid Action on Neural Circuit for Song Learning and Plasticity
The anterior forebrain circuit is essential for song learning and adult song plasticity, as well as playing a role in song perception. This pathway consists of projections from HVC to area X in the striatum, from X to the dorsolateral division of the medial thalamus (DLM), from DLM to the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), and finally to RA (Figure 1). Area X is homologous to the mammalian basal ganglia (Luo, Ding, & Perkel, 2001). LMAN neurons that project to RA send collaterals to area X, providing the potential for feedback within this pathway. The projections within this circuit are topographically organized (Foster, Mehta, & Bottjer, 1997). Inactivation of LMAN, DLM, or area X in juveniles prevents the development of normal song, but does not disrupt previously crystallized song in adults (Bottjer, Miesner, & Arnold, 1984; Halsema & Bottjer, 1992; Scharff & Nottebohm, 1991; Sohrabji, Nordeen, & Nordeen, 1990). Juvenile males with lesions of area X persist in producing songs that are variable in structure, as though they are unable to crystallize. In contrast, if LMAN is lesioned in juvenile males, they produce songs with aberrant but stable structure.
Androgen receptors are expressed at high levels in LMAN and DLM neurons, as well as in HVC and RA. AR mRNA was reported to be expressed at low levels in area X in one study (Bernard, Bentley, Balthazart, Turek, & Ball, 1999). The area X-projecting neurons in HVC contain either AR or ER (Johnson & Bottjer, 1993, 1995; Sohrabji et al., 1989), but individual X-projecting neurons express only one of these receptor types (Frankl-Vilches & Gahr, 2018; Gahr, 1990).
Sex Steroids Modulate Signal Perception and Behavioral Responses
Increases in sex steroid levels in the blood and/or locally synthesized E2 in the brain during the breeding season can modulate the activity of neural circuits involved in signal perception, in motivation to respond to signals with aggressive or sexual behaviors, and in reproductive priming. In frogs, fishes, and birds, peripheral and central auditory processing systems exhibit seasonal changes in activity that are associated with changes in reproductive state (reviewed in Caras & Remage-Healey, 2016; Forlano et al., 2016; Wilczynski & Burmeister, 2016). Steroid modulation of auditory activity ensures that receivers will be responsive to the acoustic mating signals produced by senders at the optimal time for reproduction.
Steroids Alter Behavioral Responses to Signals
It is widely observed across vertebrate taxa that males in reproductive condition respond aggressively when they detect the advertisement signals of other males of the same species. Aggressive responses to signals are typically modulated by circulating androgen levels, though the relationship between aggression and T levels can change with season, stage of breeding, parenting status, and social familiarity among individuals (Oliveira, 2004; Wingfield et al., 1994). Castrated males, and males treated with androgen antagonists, generally are less aggressive in response to other males’ signals, and less successful at defending territories against other males during the breeding season (Jalabert et al., 2018; Wingfield, 1994).
Female birds of numerous species perform copulation solicitation displays in response to conspecific, but not heterospecific, songs when in reproductive condition (reviewed in Catchpole & Slater, 2008). Outside the breeding season, female birds do not perform sexual displays to male song. Female canaries in breeding condition built nests more rapidly when exposed to playback of conspecific rather than heterospecific song, and when exposed to more complex canary song than simpler song (Kroodsma, 1976). The response of female Tungara frogs (Physalaemus pustulosus) to conspecific male calls changed with hormonal condition (Lynch, Crews, Ryan, & Wilczynski, 2006). Female frogs showed their strongest phonotaxic approach to playbacks of male calls when circulating levels of estrogen and progesterone peaked (Lynch & Wilczynski, 2005).
The behavioral response of males and females to signals may change with their hormonal levels. During the breeding season, territorial male Red-winged Blackbirds and White-crowned Sparrows (Zonotrichia leucophrys) respond aggressively to the songs of other males (reviewed in Catchpole & Slater, 2008). Female blackbirds and sparrows in reproductive condition respond to conspecific male song by soliciting copulations (Searcy & Brenowitz, 1988; Searcy & Marler, 1984). Outside the breeding season, however, when redwings and sparrows forage and roost in large groups, male song becomes an attractive signal and individuals of both sexes approach singing males (Brenowitz, 1981).
Steroids Act on Neural Circuits for Signal Perception
Hormones act on receptors in auditory end organs and central auditory neurons to modulate their sensitivity and activity in response to acoustic signals across vertebrates. Similar effects of sex steroids on sensory receptors and neurons are seen in weakly electric fish (Smith, 2013; Zakon, 1998).
ER are present in hair cells of auditory end organs in fish (sacculus), birds, and mammals (cochlea), ER are present in the auditory nerve spiral ganglion cell bodies of fish and mammals, and AR are found in the spiral ganglion of birds (Forlano et al., 2016; Noirot et al., 2009; Stenberg, Wang, Sahlin, & Hultcrantz, 1999). Neurons in auditory nucei in the brainstem and midbrain express ER or, to a lesser degree, AR in different vertebrates. Steroid receptors may be sparse or absent in thalamic and primary telencephalic auditory regions, including nucleus ovoidalis and Field L in birds (Caras, 2013; Forlano et al., 2016; Voigt, Ball, & Balthazart, 2009). Telencephalic secondary auditory regions may express ER (e.g., medial caudal nidopallium, NCM, in birds) or AR (e.g., dorsal medial telencephalon in fish; Caras, 2013; Forlano et al., 2016).
Sex steroids act on auditory neurons to modulate their sensitivity to stimulation by, and/or level of activity in response to, conspecific signals. Female midshipman fish (Poricthys notatus) become more sensitive to harmonic frequencies contained in male advertisement calls as their blood levels of E2 and T rise at the onset of the breeding season (Forlano et al., 2016). Female African cichlid fish (Astatotilapia burtoni) in reproductive condition are more sensitive to sound frequencies present in male courtship signals, and there is a correlation between circulating levels of E2 and hearing thresholds (Maruska, Ung, & Fernald, 2012). Hearing conspecific song increases local E2 synthesis in NCM of Zebra Finches, which then increases sound-evoked neuronal activity and auditory response strength (Remage-Healey, Coleman, Oyama, & Schlinger, 2010). E2 treatment of female White-crowned Sparrows increases conspecific song-evoked activity in neurons in Field L, and expands the range of sound intensities over which song stimuli elicit responses (Caras, O’Brien, Brenowitz, & Rubel, 2012). This effect of E2 on activity in Field L neurons is particularly interesting because these cells do not express steroid receptors; hormone modulation may result from steroid effects on auditory nuclei upstream in the sensory circuit, and/or by dopaminergic projections from the central grey (CG), substantia nigra (SN), and ventral tegmental area (VTA) to auditory regions of the brainstem, thalamus, and telencephalon (Appeltants, Absil, Balthazart, & Ball, 2000; Matragrano et al., 2012). Neurons in the CG, SN, and VTA are sensitive to sex steroids (Purves-Tyson et al., 2012; Sipos & Nyby, 1996).
Steroids Act on Neural Circuits that Mediate Aggressive Responses to Signals
The neural circuit that mediates aggressive behavior is conserved across vertebrates, and includes the medial amygdala (nucleus taeniae in birds), the bed nucleus of the stria terminalis (BNST), the lateral septum (LS), the POM, the anterior hypothalamus (AH), the ventromedial hypothalamus (VMH), and CG/ICo (Jalabert et al., 2018). Neurons in each of these brain regions express AR and/or ER. It has been shown in frogs, lizards, and birds that POM and different hypothalamic regions receive auditory input from midbrain and thalamic auditory nuclei (Bruce & Neary, 1995; Hoke, Ryan, & Wilczynski, 2005; Wild, 2017). The extensive connectivity between sub-regions confers auditory sensitivity throughout the hypothalamus. Auditory information is conveyed from the AH and VMH to other nuclei in the circuit for aggression. The auditory sensitivity of neurons throughout this circuit to conspecific signals is modulated by binding of sex steroids, and this provides a neural basis for the observed hormone sensitivity of aggressive responses shown by animals when they detect the signals of other conspecifics.
Signal Perception Can Prime the Reproductive System
Acting through the hypothalamic–pituitary–gonadal axis (HPGA) and the release of gonadotrophin-releasing hormone (GnRH), detection of auditory signals can stimulate testicular and ovarian development (Oliveira, 2004; Wingfield et al., 1994). Perception of conspecific, but not heterospecific, calls stimulates testicular development in males of different frog species (reviewed in Leary, 2009). The rate of seasonal testis growth, and circulating T levels, in male birds of several species have been shown to increase in the presence of females in reproductive condition (reviewed in Wingfield et al., 1994). Detection of conspecific male calls has been shown to stimulate ovarian development, sexual receptivity, and/or circulating E2 levels in female frogs (reviewed in Leary, 2009). In female birds of several species, exposure to a live male producing courtship signals, or to playback of conspecific, but not heterospecific, vocalizations stimulates growth of the ovaries and oviduct in females (reviewed in Wingfield et al., 1994). Auditory sensitivity of hypothalamic neurons thus provides a substrate for interactions between signal perception, hormones, behavioral motivation, and reproductive priming (Hoke et al., 2005).
Auditory end organ:
an anatomical structure that contains the primary sensory receptors (hair cells in vertebrates) that transduce acoustic energy to neural activity.
the third stage in the motor phase of song learning, when birds produce a well-structured, stereotyped version of the conspecific song model to which they were exposed during the earlier memory acquisition phase.
alteration of ongoing behavior or neural activity
the physiological drive that initiates behavior in response to an internal or external stimulus
a suborder of birds in the order Passeriformes, also referred to as “songbirds”
the processing and identification of sensory input.
the second stage in the motor phase of song learning. Plastic song is louder and better structured than subsong, but still variable in form.
in vertebrate embryos, a transient constricted swelling of the neural tube that gives rise to the hindbrain
the first major phase of song learning, which occurs when a bird listens to and memorizes songs produced by adult conspecific birds.
the second major phase of song learning, which involves ongoing comparison between a sensory model of song acquired during an earlier memorization phase and auditory feedback from a bird’s own production of song.
the first stage in the motor phase of song learning. Subsong is quiet, poorly structured, and very variable in form.
a sensory model of song acquired during the initial memory phase of song learning. A bird compares auditory feedback from its own singing with this sensory model to gradually improve song quality to eventually match the template.
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