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Reproduction and vocalization in midshipman fish are closely interlinked. Mating in midshipman fish depends on auditory communication, the production and reception of sound signals. Males produce several different vocalizations, while females only make grunts in non-breeding situations. [1]
Typical Type I male calls are divided into short grunts that last for milliseconds or are produced in a series of grunts called a "grunt train", mid-duration growls, and long duration advertisement hums that can last up to an hour. [2] These calls can be recorded naturally. They can also be produced in a laboratory, a procedure known as "fictive calling". [3] [4] In nature, two muscles contracting on the swim bladder produce these sounds. In the laboratory, sounds are produced by a stimulating electrode placed on the periaqueductal gray (PAG) and a recording electrode placed on the occipital nerve that leads to the sonic muscles of the fish. [4] [5]
The vocalizations of male midshipman fish are androgen and estradiol steroid mediated. There are high blood levels of these hormones during the transition from non-calling to calling before midshipman breeding season, [6] suggesting that higher hormone levels are needed for making advertisement calls. Feeding 11-ketotestosterone coated scallops to toadfish increases their calling behavior, [7] which identifies 11-ketotestosterone, an androgen hormone, as a mediator of midshipman fish vocalization. There are also high levels of aromatase, an estrogen-generating enzyme, in the hindbrain vocal motor region. Estradiol steroids and their receptors are present in the same areas already concluded to be involved in male midshipman calling. [8]
There are three genders of midshipman fish: females, type I males, and type II males. Type I and type II males have different reproductive strategies, and can be distinguished from each other based on physical characteristics. Type I males are eight times larger in body mass, and have much larger vocal organs. Type II males’ reproductive organs are seven times larger in size than those of type I males. [1] Female and type II male midshipman fish can be distinguished from each other by the female's slightly larger size, and the type II male midshipman's large reproductive organs. [3]
The three genders of midshipman fish have different steroid-mediated reproductive behaviors. Type I territorial males use vocalizations via paired muscles in the swimming bladder to attract females, while type II males invest in larger reproductive organs. [1] Type II males then “sneak” into nests because they look much like females and fertilize laid eggs. This behavior is referred to as cuckoldry or satellite-spawning. [3] Type II males and females are incapable of long duration calls. [9] 11-Ketotestosterone is the major steroid present in Type I males’ vocalization systems, while Type 2 males’ and females’ vocalizations are primarily mediated by testosterone. [10] The specific mechanisms by which these steroids act are still unknown. [8]
The sounds produced by male midshipman fish cause reproductive females to develop a hormone-mediated selective sensitivity to this sound, and they respond by laying eggs in the rock nest of a singing male. This selective sensitivity to higher frequency correlates to increased levels of testosterone and estradiol. [11]
The neuronal pathway for midshipman vocalization starts at the ventral medullary nucleus and continues to a hindbrain vocal pattern generator, which contains both pre-pacemaker and pacemaker nuclei. [4] For each action potential fired in their vocal pattern generator, there is exactly one sonic motor neuron that fires, and there is exactly one sound pulse. [12] The two motor nuclei fire in phase in toadfish, leading to the paired contraction of the sonic muscles. [13]
The duration of calls is controlled by the pre-pacemaker neurons in the hindbrain. The duration is encoded by a long depolarization of these pre-pacemaker neurons. Exposing pacemaker neurons to different levels of the anesthetic lidocaine alters the duration of the calls, but not the frequency Pacemaker neurons code for the frequency of signals using "ultrafast" rhythmic oscillations in membrane potential. As midbrain stimulus increased, the oscillations increased in amplitude. [5]
Although midshipman fish have been known to wake houseboat owners, [14] research surrounding their vocalizations could be beneficial to humans. Midshipman fish are model organisms for studying both human speech and hearing. Recently, it was found that midshipman fish can decrease their own hearing sensitivity by stiffening their inner ear hair cells while they are vibrating their calling muscles. [15] This behavior is also found in bats, and may lead to an understanding a similar mechanism humans use to turn down their ear sensitivity to retain their hearing longer. [14] There are conserved patterns of vocal, auditory, and neuroendocrine mechanisms between teleosts and tetrapods, which include midshipman fish and humans, respectively. This model organisms’ simple system could lead to a deeper understanding of human speech and auditory pathways,. [1] [5] [16] This evolutionary connection could be important in modern medicine because these fish have homologous brain structures to humans. An example is for patients with lesions in the brain that become mute after having a stroke. [17] [18]
On August 9, 1974, composer Charlie Morrow performed a concert for fish using what he understood to be decoded toadfish language, similar to his decoded field peeper language. Morrow observed that choruses of multiple toadfish shift leadership based on call and response by strong individuals. He notated the patterns for human performance, in one version numbering each individual for identification and spatial location. The night before, Richard Nixon resigned as U.S. president. Major media covered the concert. New York Times music critic, John Rockwell, wrote a review with the headline, "Fish Silent". [19]
Midshipman fish have two forms of males: the nest-building Type I and "sneaker male" or "satellite male" Type II. [20] Type I males attract females to their nests with their humming, coax them to lay eggs, and guard them. [20] In contrast, Type II males do not build nests or attract females on their own. [20] Instead, they sneak up to the Type I's nests and deposit their eggs. [20] These behavioral differences can be seen in the differences in the structure and function of the nervous system. [17]
Type I males and Type II males and females grow along different growth paths when it comes to neurons and muscles that determine morph-specific vocal behavior. [17] For Type I males, for example, sexual maturation is preceded by growth of the mate-calling circuit and sonic muscle. [21] Specifically, before the transformation from juvenile to type I male, the size of the motoneurons and volume of the sonic motor nucleus increases twofold and the number of sonic muscle fibers increases fourfold. [17] At the start of sexual maturation, the motoneurons increase in size again, although not as much as before. [17] The pacemaker neurons also increase in size at this time but not as much as the motoneurons in general. [17] The sonic muscle also increases fivefold in the size of muscle fibers. [17] In contrast, there is little dramatic change seen before the transformation from juvenile to type II male or adult female. In fact, the vocal neurons and muscles change little or not at all.
Differences between the reproductive strategies of Type I and Type II are also reflected in hormonal differences during sexual maturation. [22] The three different morphs – Type I, Type II, and females – also produce different levels of various hormones. [17] Type II males produce the highest levels of testosterone, followed by females and then Type I males. [17] Females only have estrogen in the form of 17β-estradiol but at much lower levels than testosterone. [17]
Type I males also have five times more 11-ketotestoterone, which is a form of testosterone common to teleosts, than type II males and females. [17] 11-ketotestosterone is likely to be more potent than testosterone in supporting courtship behaviors such as humming. [22]
Estrogen, or oestrogen, is the primary female sex hormone. It is responsible for the development and regulation of the female reproductive system and secondary sex characteristics. There are three major endogenous estrogens in females that have estrogenic hormonal activity: estrone, estradiol, and estriol. The estrane steroid estradiol is the most potent and prevalent of these.
Testosterone is the primary male sex hormone and anabolic steroid. In male humans, testosterone plays a key role in the development of male reproductive tissues such as testes and prostate, as well as promoting secondary sexual characteristics such as increased muscle and bone mass, and the growth of body hair. In addition, testosterone is involved in health and well-being, and the prevention of osteoporosis. Insufficient levels of testosterone in men may lead to abnormalities including frailty and bone loss.
The hypothalamus is a portion of the brain that contains a number of small nuclei with a variety of functions. One of the most important functions of the hypothalamus is to link the nervous system to the endocrine system via the pituitary gland. The hypothalamus is located below the thalamus and is part of the limbic system. In the terminology of neuroanatomy, it forms the ventral part of the diencephalon. All vertebrate brains contain a hypothalamus. In humans, it is the size of an almond. The hypothalamus is responsible for the regulation of certain metabolic processes and other activities of the autonomic nervous system. It synthesizes and secretes certain neurohormones, called releasing hormones or hypothalamic hormones, and these in turn stimulate or inhibit the secretion of hormones from the pituitary gland. The hypothalamus controls body temperature, hunger, important aspects of parenting and attachment behaviours, thirst, fatigue, sleep, and circadian rhythms. The hypothalamus derives its name from Greek ὑπό, under and θάλαμος, chamber.
An androgen is any natural or synthetic steroid hormone that regulates the development and maintenance of male characteristics in vertebrates by binding to androgen receptors. This includes the embryological development of the primary male sex organs, and the development of male secondary sex characteristics at puberty. Androgens are synthesized in the testes, the ovaries, and the adrenal glands.
Luteinizing hormone is a hormone produced by gonadotropic cells in the anterior pituitary gland. In females, an acute rise of LH triggers ovulation and development of the corpus luteum. In males, where LH had also been called interstitial cell–stimulating hormone (ICSH), it stimulates Leydig cell production of testosterone. It acts synergistically with follicle-stimulating hormone (FSH).
Bird vocalization includes both bird calls and bird songs. In non-technical use, bird songs are the bird sounds that are melodious to the human ear. In ornithology and birding, songs are distinguished by function from calls.
Gonadotropin-releasing hormone (GnRH) is a releasing hormone responsible for the release of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from the anterior pituitary. GnRH is a tropic peptide hormone synthesized and released from GnRH neurons within the hypothalamus. The peptide belongs to gonadotropin-releasing hormone family. It constitutes the initial step in the hypothalamic–pituitary–gonadal axis.
5α-reductases, also known as 3-oxo-5α-steroid 4-dehydrogenases, are enzymes involved in steroid metabolism. They participate in 3 metabolic pathways: bile acid biosynthesis, androgen and estrogen metabolism. There are three isoenzymes of 5α-reductase, SRD5A1, SRD5A2, and SRD5A3, which vary in different tissues with age.
Thalassoma bifasciatum, the bluehead, bluehead wrasse or blue-headed wrasse, is a species of marine ray-finned fish, a wrasse from the family Labridae. It is native to the coral reefs of the tropical waters of the western Atlantic Ocean. Individuals are small and rarely live longer than two years. They form large schools over the reef and are important cleaner fish in the reefs they inhabit.
The hypothalamic–pituitary–gonadal axis refers to the hypothalamus, pituitary gland, and gonadal glands as if these individual endocrine glands were a single entity. Because these glands often act in concert, physiologists and endocrinologists find it convenient and descriptive to speak of them as a single system.
Midshipman fish belong to the genus Porichthys of toadfishes. They are distinguished by having photophores and four lateral lines. Typical midshipman fishes, such as the plainfin midshipman, are nocturnal and bury themselves in sand or mud in the intertidal zone during the day. At night they float just above the seabed. Some species have venomous dorsal spines and are capable of inflicting serious injuries if handled.
Adrenosterone, also known as Reichstein's substance G , as well as 11-ketoandrostenedione (11-KA4), 11-oxoandrostenedione (11-OXO), and androst-4-ene-3,11,17-trione, is a steroid hormone with a weak androgenic effect, and an intermediate/prohormone of 11-ketotestosterone. It was first isolated in 1936 from the adrenal cortex by Tadeus Reichstein at the Pharmaceutical Institute in the University of Basel. Originally, adrenosterone was called Reichstein's substance G. Adrenosterone occurs in trace amounts in humans as well as most mammals and in larger amounts in fish, where it is a precursor to the primary androgen, 11-ketotestosterone.
Astatotilapia burtoni is a species of fish in the family Cichlidae.
Anabolic steroids, also known more properly as anabolic–androgenic steroids (AAS), are steroidal androgens that include natural androgens like testosterone as well as synthetic androgens that are structurally related and have similar effects to testosterone. They are anabolic and increase protein within cells, especially in skeletal muscles, and also have varying degrees of androgenic and virilizing effects, including induction of the development and maintenance of masculine secondary sexual characteristics such as the growth of facial and body hair. The word anabolic, referring to anabolism, comes from the Greek ἀναβολή anabole, "that which is thrown up, mound". Androgens or AAS are one of three types of sex hormone agonists, the others being estrogens like estradiol and progestogens like progesterone.
11-Ketotestosterone (11-KT) is an oxidized form of testosterone that contains a keto group at the C11 position. It is related to adrenosterone, an androgen found in trace quantities in humans. In fish, 11-ketotestosterone functions as the endogenous androgenic sex hormone. In midshipman fish, 11-ketotestosterone is not present in females or Type II Males — Type II Males reach sexual maturation later, are less territorial, and have higher testosterone than Type I Males.
Prenatal Testosterone Transfer refers to the phenomenon in which testosterone synthesized by a developing male fetus transfers to one or more developing fetuses within the womb and influences development. This typically results in the partial masculinization of specific aspects of female behavior, cognition, and morphology, though some studies have found that testosterone transfer can cause an exaggerated masculinization in males. There is strong evidence supporting the occurrence of prenatal testosterone transfer in rodents and other litter-bearing species, such as pigs. When it comes to humans, studies comparing dizygotic opposite-sex and same-sex twins suggest the phenomenon may occur, though the results of these studies are often inconsistent.
Hypogonadotropic Hypogonadism (HH), is due to problems with either the hypothalamus or pituitary gland affecting the hypothalamic-pituitary-gonadal axis. Hypothalamic disorders result from a deficiency in the release of gonadotropic releasing hormone (GnRH), while pituitary gland disorders are due to a deficiency in the release of gonadotropins from the anterior pituitary. GnRH is the central regulator in reproductive function and sexual development via the HPG axis. GnRH is released by hypothalamic neuroendocrine cells into the hypophyseal portal system acting on gonadotrophs in the anterior pituitary. The release of gonadotropins, LH and FSH, act on the gonads for the development and maintenance of proper adult reproductive physiology. LH acts on Leydig cells in the male testes and theca cells in the female. FSH acts on Sertoli cells in the male and follicular cells in the female. Combined this causes the secretion of gonadal sex steroids and the initiation of folliculogenesis and spermatogenesis. The production of sex steroids forms a negative feedback loop acting on both the anterior pituitary and hypothalamus causing a pulsatile secretion of GnRH. GnRH neurons lack sex steroid receptors and mediators such as kisspeptin stimulate GnRH neurons for pulsatile secretion of GnRH.
Porichthys notatus is a species of fish in the toadfish family. It is a midshipman known by the common name plainfin midshipman. It is native to the eastern Pacific Ocean, where its distribution extends along the coast from Sitka, Alaska, to Magdalena Bay in southern Baja California.
Behavioral Endocrinology is a branch of endocrinology that studies the Neuroendocrine system and its effects on behavior. Behavioral endocrinology studies the biological mechanisms that produce behaviors, this gives insight into the evolutionary past. The field has roots in ethology, endocrinology and psychology.
Elizabeth Adkins-Regan is an American comparative behavioral neuroendocrinologist best known for her research on the hormonal and neural mechanisms of reproductive behavior and sexual differentiation in birds. She is currently a professor emeritus in the Department of Psychology and the Department of Neurobiology and Behavior at Cornell University.