Social Behaviors in Fish, Part 1: Social Systems and Sex Change

[Harlequinmania]

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It’s not just aquarium hobbyists that find the behaviors of fish fascinating. The vast diversity of social systems and mating strategies within teleost fish has long inspired scientific research. Fish exhibit more variation in social systems and mating strategies than any other vertebrate group [1]; from polygyny (having many mates), to monogamy (having one mate), to sex changers with dominant males, and sex changers with dominant females, as well as an extensive array of parental care strategies. Many fishes have developed highly tuned social perceptions specific to each dynamic system. The social behaviors of fish have been studied as alternative model behavioral systems for decades.

So why study fish? The highly complex social structures are easily manipulated. In several of these systems, social context gives precise signals that engender changes in physiology, reproduction, and behavior.  The very tractable endpoints of these socially induced behaviors (i.e. sex change, behavioral shifts, and coloration changes) are easily measured and therefore provide excellent data. Fish are also excellent aquarium inhabitants, showing natural behaviors unrestricted by captivity; along with short generation times and high reproductive capacity, fish make excellent model systems in studying behavior. Science has also shown us that much of the underlying neuroendocrine mechanisms that facilitate fundamental behaviors such as aggression, mating, reproduction, and parental care, are highly conserved across vertebrates. In other words, the neurons, peptides, hormones, and signaling pathways which regulate many of these behaviors are homologous, having a shared ancestry across evolutionary time [2].

In Freshwater Fish

Perhaps the most studied species is the freshwater cichlid, Astatotilapia burtoni, common in many aquariums, but also well known for its contribution to our understanding of how social circumstances shape the brain and behavior.  The burtoni cichlid has a polygynous mating system, where dominant males have access to a territory and several females. Dominant males are brightly colored, highly aggressive, and have many physiological differences from subordinate males [3]. Subordinates males are drab in color and do not hold territories. They are almost indistinguishable from females and are lacking reprodu­ctive capabilities.

Dominant male Astatotilapia burtoni showing characteristic bright coloration and black eye bar.  Photos by Karen Maruska.

Subordinate male Astatotilapia burtoni, note the lack of an eye bar and drab coloration. These males can switch back and forth between morphs depending on social circumstances.

What is so fascinating about this system is the phenotypic plasticity among dominant and subordinate males.  Dominant and subordinate males switch back and forth depending on the social circumstances. Within minutes of removing a dominant male from a territory, a subordinate male will rise in rank. Over a short time, changes in the brain occur, colors will change, gonads enlarge, hormone levels differ, and reproductive capabilities will develop [4]. However, there are costs to being dominant, due to their conspicuous coloration dominant males are under much higher predation risk. More time and energy is spent defending territories, while less effort is used feeding. Under stressful social circumstances, dominant individuals will be suppressed by rising subordinates, and move back down the hierarchy, losing their bright coloration, and undergoing a variety of hormonal and behavioral changes. These remarkable morphological transitions are based on the interpretation of complex social cues from conspecifics within the social system.

In Marine Fish

Unlike freshwater species, in many marine species, shifts in social status are often associated with sex change; one of the most dramatic physiological transitions in the animal kingdom. Like the dominant and subordinate changes that occur in A. burtoni, similar social complexities regulate changes of the social hierarchy in many saltwater fish, but accompanying these changes in social position are changes in sexual morphology. Among vertebrates, only mammals and birds display universal genetically controlled sex predetermined at the time of fertilization. After gonads have developed, they influence the morphology and physiology of the brain and body (i.e. masculinization and feminization). In many marine fish, the process is reversed. Social cues interpreted by the brain then signal to the gonads to differentiate as male or female during development [5].

This photo shows the incredible color change that occurs between Initial phase males (above), and terminal phase males (below) of the Bluehead wrasse.

The most studied of the sex changing species within the scientific literature are the Bluehead wrasse and Blue-banded goby.  The Bluehead wrasse is a protogynous hermaphrodite, meaning that they start out as females, and then, depending on social context can change sex into a male later on in life. The Bluehead wrasse, regardless of sex, displays either one of two color types: initial phase (IP), and terminal phase (TP). Females are always in the IP coloration, while males can either display IP, or TP coloration [6]. These phases are consistent with terminology that describes many wrasses in the aquarium hobby (you’ve probably noticed a higher price tag when you see ‘TP’ following a listing).  Sex change in this species occurs quite rapidly, within minutes of TP male removal behavior patterns of rising subordinates shift, within a day coloration begins to change, and in under 10 days individuals previously spawning as females can produce sperm, and reproduce as males [7].  There is an allure of keeping many in individuals of one species in a tank, for example, having several anthias (another protogynous species) makes its much more likely to see natural behavioral interactions between males and females than having just one alone.  In flasher wrasses, the ‘flash’ from terminal phase males occurs almost exclusively in the presence of conspecific females.

Another interesting system is the Blue-banded goby, or Catalina goby as it is often referred in the hobby.  This species is a polygynous bidirectional hermaphrodite; populations consist of pure females, pure males, and simultaneous hermaphrodites biased toward both sexes [8]. Here, males ‘rule’ a harem of females; when the dominant male is removed, a female will change sex to take its place.  If another male subordinates a dominant male, the dominant individual is also able to revert its sex back to female. In this species both protogyny (sex change from female to male), and protandry (sex change from female to male) can be studied, and these transitions have been well detailed in the laboratory. Without color changes or obvious visual size differences, the length to width ratio of the genital papilla determines sexual phenotype, with males having a ratio > 1.6 and females around 1.  In laboratory controlled all male groups, one dominant male will emerge. All other males will revert to female, and fertilized eggs can appear within 16 days.  In all female groups, the opposite occurs, a dominant female will change sex into male, while all other subordinate individuals will remain female [9].

Although the end product of changes in behavior, coloration, gonads, and ultimately sex are understood, the underlying biology that facilitates this process is not.  How social signals are processed in the brain, and how those neural networks then signal through the various physiological systems ultimately leading to complete sex change has been an intriguing subject of study.

An interesting contrast to these polygynous groups with dominant individuals being male is perhaps the most popular of all aquarium fish: the monogamous clownfish.

Clownfish are unique in their life histories as they are obligate symbionts with anemones.  This peculiar relationship leaves them spatially restricted. As poor swimmers, and lacking any predatory defenses, leaving after establishing themselves on an anemone, or colony of anemones (depending on the anemone species), would be a poor survival decision.  Unlike wrasses, where mates may be more available, clownfish have developed a monogamous mating system. One dominant female presides over a territory while paired with a subordinate male.  In monogamous bonds the pair produces a greater number of gametes if the larger individual is female, and in most organisms, especially fish, larger individuals are dominant [10]. While other clownfish may also inhabit the anemone in the natural environment, these individuals, like subordinated male cichlids and wrasses, have reduced gonadal structures and are non-reproductive. Here, sex change is not as expeditious as in the wrasse, or Blue-banded goby, but has been recorded to occur within 45 days in the wild [11]. While no obvious color changes occur, drastic behavioral, endocrine, and size changes transpire. This species is also an interesting system due in part to that fact that gonads consisting of predominantly testicular tissue transition to ovarian tissue, and these gonadal transitions predict opposite changes in androgen levels, as dominant more aggressive individuals are female [12].

Stained ambisexual gonad of a juvenile clownfish (sp. A. ocellaris)

These contrasting social systems: the male dominant sex changing Bluehead wrasse, the female dominant sex changing clownfish, the bidirectional Blue-banded goby, and the plastic male phenotypes of the burtoni cichlid are useful compliments to one another.  Using these different systems researchers are able to dissociate physiological pathways that may be involved in maleness vs. dominance, as well as untangling the underpinning mechanisms in sex change from male to female vs. sex change from female to male.

Fish have been an important group in understanding the neurobiology of social behaviors. Many of the basic behaviors that have inspired research in psychology, neuroscience, and animal behavior are displayed across fish. Along with these behavioral displays, the beautiful coloration and charismatic qualities of fish make them fun to keep and study alike.

 

References:

1. Frisch, A., Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish. Reviews in Fish Biology and Fisheries, 2004. 14(4): p. 481-499.
2. O'Connell, L.A. and H.A. Hofmann, Evolution of a vertebrate social decision-making network. Science, 2012. 336(6085): p. 1154-1157.
3. Neumeister, H., et al., Social and ecological regulation of a decision-making circuit. J Neurophysiol, 2010. 104(6): p. 3180-8.
4. O'Connell, L.A., et al., Neuroendocrine mechanisms underlying sensory integration of social signals. J Neuroendocrinol, 2013. 25(7): p. 644-54.
5. Elofsson, U., S. Winberg, and R.C. Francis, Number of preoptic GnRH-immunoreactive cells correlates with sexual phase in a protandrously hermaphroditic fish, the dusky anemonefish (Amphiprion melanopus). Journal of Comparative Physiology A, 1997. 181(5): p. 484-492.
6. Marsh, K.E., et al., Aromatase immunoreactivity in the bluehead wrasse brain, Thalassoma bifasciatum: Immunolocalization and co-regionalization with arginine vasotocin and tyrosine hydroxylase. Brain Research, 2006. 1126(1): p. 91-101.
7. Warner, R.R. and S.E. Swearer, Social control of sex change in the bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). The Biological Bulletin, 1991. 181(2): p. 199-204.
8. Mary, C.S., Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction. Behavioral Ecology, 1994. 25(2): p. 301-314.
9. Rodgers, E., R. Earley, and M. Grober, Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. Journal of Fish Biology, 2007. 70(6): p. 1660-1668.
10. Avise, J. and J. Mank, Evolutionary perspectives on hermaphroditism in fishes. Sexual Development, 2009. 3(2-3): p. 152-163.
11. Godwin, J.R. and P. Thomas, Sex Change and Steroid Profiles in the Protandrous Anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). General and Comparative Endocrinology, 1993. 91(2): p. 144-157.
12. Godwin, J., Behavioural aspects of protandrous sex change in the anemonefish, Amphiprion melanopus, and endocrine correlates. Animal Behaviour, 1994. 48(3): p. 551-567.

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