Sexual Differentiation of Cichlids

Figure 1.While these cichlids may appear to be kissing, do not be fooled. Much like humans, this male and female pair are actually having a small spat and are solving their differences through mouth fighting, a common demonstration of aggression in cichlids. (The Convict Cichlid)

Sexual Lability

Have you ever looked into your fishbowl and wondered if your goldfish was male or female?  The question with the far more interesting answer: how did the fish actually become male or female? Sexual differentiation in fish, namely cichlids in these studies, has been long studied due to its complexity and dependence on multiple factors.  Cichlids have great variability in the timing of sexual differentiation, and different species have differing sexual lability over time as shown in Figure 2. This sexual lability is a sort of plasticity that allows them to change sexes (from male to female or female to male) as the circumstances in which they survive change. In fact, “there are more reports of various expression of sexual lability in [cichlids] than in other groups of freshwater fishes.” (Oldfield et al., 2005)

Figure 2. Sexual lability in different cichlid species at various life stages. (Oldfield et al., 2005) The X's indicate presence of sex differentiation in the species, while the 0's indicate absence.

Figure 3. Sexual lability over cichlid lifespan (Oldfield et al,. 2005)

As shown in Figure 3, sexual lability occurs in four different phases:

  1. The first phase occurs during fertilization, and sex is solely determined by the zygote’s genetic composition. This is the most familiar sexual lability due to its commonality.
  2. The second phase occurs during the larval stage of the life cycle, and certain environmental factors such as temperature and pH affect the organism’s sexual identity.
  3. The third phase occurs during the juvenile stage, where sexual identity is determined by certain social cues such as the size of other cichlids in the community.
  4. The fourth phase occurs during adulthood, when the cichlid experiences sequential hermaphroditism. This means that the cichlid is born one sex, but changes sexes at adulthood. After the hermaphroditic changes take place, the fish either has both male and female germ cells in the gonads, or the gonads completely change from one sex to the other.

Overall, these studies could prove invaluable to fish farmers during breeding season, especially those who raise cichlids such as tilapia. The farmers may want to artificially change the sex of some of their crop in order to produce the highest yield possible.  The results of these studies could also be used to help understand the development of other organisms who have similar sexual lability, like gastropods and plants.

Genetic Factors

First and foremost, genetics has a strong pull in the sexual differentiation of the cichlid. This lability factor is determined at fertilization. At least 4 distinct sex chromosomes have been identified in cichlid fish, and many remain unknown.  A study by Jennifer Ser determined that Malawi cichlids have both a ZW system on linkage group 5 and an XY system on linkage group 7. In the ZW system, the ovum is the sex determining gamete as opposed to the sperm in the XY system. (Figure 4)  A male would be indicated by ZZ and a female by ZW.  When both a ZW and XY system are present, epistasis dictates that the ZW system predominates. (Ser et al., 2009) While ZZXX individuals are usually female, additional sex-determining loci can cause them to differentiate as males. So no matter how the ZW or XY system classifies the cichlid, their sex may change if another locus overrides its effects.  The best explanation for all of these sex-determining loci in cichlids is that they are a response to sexually antagonistic selection.  “Alleles that increase the fitness of one sex, but decrease the fitness of the opposite sex, create a genetic conflict which can be resolved by linkage to a nearby sex-determining locus.” (Oldfield et al., 2011) Genetic sex can also be overridden by early treatment with exogenous hormones.

Figure 4. ZW and XY systems and how they determine gender. (Dementyeva, E.V., and Zakian, S.M., 2012)

Environmental Factors

Environmental sex determination of cichlids occurs during the larval stage of the cichlid life cycle.  Such factors that have been tested in laboratory settings include temperature and pH. Romer and Beisenherz studied the effects of temperature and pH on 37 species of  Apistogramma, a specific genus of cichlids. (Figure 5)  They found that temperature and pH greatly affected 33 of the species. Lower incubation temperatures of larva (23 degrees Celsius) produced female fish, higher temperatures (29 degrees Celsius) produced male fish, while an intermediate temperature (26 degrees Celsius) yielded a 1:1 sex ratio. In the same setup, acidic water (pH 4-5) yielded 90% males and neutral water (pH 7.0) yielded 90% females. Sex was determined using secondary sex characteristics. Perhaps male fish survive better or are more fertile in warmer, more acidic environments, and it is an evolutionary mechanism that these conditions stimulate their development.

Figure 5. Apistogramma nijsseni, a popular aquarium pet of Dwarf cichlid enthusiasts. ("Apistogramma," 2012)

Social Factors

Social cues, namely size of other cichlids in the surrounding environment, have also been shown to affect sexual differentiation. Ali et al. observed the growth of two groups of cichlids, separated by small and large size, over a period of 6 months. If genetic factors alone controlled the sex of the fish, the group with the small individuals would be expected to be all female, and the group with large individuals would be expected to be all male. (Figure 6 demonstrates the size differences between the sexes.) However, without the aggressive behavior of the larger fish, the smaller fish were able to grow equally as large as the large group.  The largest fish of both groups were male, and the females were smaller. (In the Midas cichlids, the male guards the nest while females raise the offspring, so the size different makes sense.)  The overall sex ratios were found to be 1:1.  This study suggests that while the female differentiation path is default, growth suppression by the larger fish represses the transformation from male to female.  While this experiment shows support for social influence in sexual differentiation, there are other factors that may be the cause.  Fish are known for their growth plasticity in response to environment, including food availability, fish density, and even effects from the tank.

Figure 6. A pair of firemouth cichlids. Note that the male is larger with long fin extensions while the female is smaller and rounder. (Coleman, R., 2012)

Hermaphroditism

There is still much controversy if cichlid sequential hermaphroditism actually occurs. Some convincing evidence comes from a study by Carruth on C. punctulata. A group of 15 young fish, all showing female coloration (checkerboard patterning) and similar size (2-3cm), were divided into small groups in 37 liter aquariums. After 6 months, each group was moved to a 110 liter aquarium for behavioral observation.   In each group, the individual showing the most dominant behavior, like tail-nipping and chasing, developed male coloring where their checkerboard pattern became a straight line.  Samples from each group were killed to check for gonad consistency with color.

A second experiment was performed by Carruth using the same fish from the previous experiment. Five adult subordinate females, three adult dominant females, and three male C. punctulata were kept in isolation for 22 weeks.  All three dominant females developed male secondary characteristics, but only one subordinant female developed them. Both experiments by Carruth show that the presence of a social hierarchy established by aggressive behaviors determines which females develop male secondary sexual characteristics.

Figure 7. Testicular tissue from a fish that was isolated as dominant and female colored. Spermatogenesis is occurring and spermatogonia and spermatids are present, but no sperm have developed. (Ali et al., 2003)

On the contrary, some cichlids demonstrate same-sex pairing without sex change. This suggests that they change sex behaviorally, but not physically.  For example, some territorial male cichlids court other non-territorial males when the non-territorial males demonstrate female coloration. (Olveira and Canario, 2001) Here is a video of typical courting behavior in cichlids:

Conclusion

Overall, the papers used for this webpage were very informative, but had definite pitfalls. In general, the papers lacked images of the cichlids before and after experimentation. Such photos would have added to the credibility of the studies. For example, the paper by Ali et al. would have benefited from pictures of the small fish before and after separate incubation to show just how much the fish grew. There was also contradiction across papers for all types of sexual lability besides genetic.  While Ali et al. supports for social sex differentiation, Oldfield (2011) claims there is no proof.  It would be interesting to continue to study this field in the future to determine if cichlids are as sexual labile as hypothesized.

Overall, the cichlid family demonstrates great flexibility in sexual differentiation, but not all cichlid species are able to differentiate at each phase of sexual lability.  They help us to truly understand how sexual differentiation can be much more complicated than just a chromosomal label.

References

Ali, M., Nicieza, A. and Wootton, R.J.  “Compensatory growth in fishes: a response to growth depression.” Fish and Fisheries 4 (2003) 147–190.

“Apistogramma.” http://en.wikipedia.org/wiki/Apistogramma. Web. 24 April 2012.

Carruth, L.L.  “Freshwater cichlid Crenicara punctulata is a protogynous sequential hermaphrodite.” Copeia (2000) 71–82.

Coleman, Ron. “Telling Males from Females.” http://cichlidresearch.com/sexingcichlids.html. Web. 24 April 2012.

“The Convict Cichlid- Proper Care, Breeding, Tips and Forum.” http://www.aqua-fish.net/show.php?h=convictcichlids. Web. 24 April 2012.

Dementyeva, E.V., and Zakian, S.M., “Dosage Compensation of Sex Chromosome Genes in Eukaryotes.” ActaNaturae. Web. 27 April 2012.

Oldfield, Ronald George. “Genetic, abiotic and social influences on sex differentiation in cichlid fishes and the evolution of sequential hermaphroditism.” Fish and Fisheries. 6 (2005) 93-110.

Oldfield, Ronald George. “Gonad development in Midas cichlids and the evolution of sex change in fishes.” Evolution and Development. 13.4 (2011) 352-360.

Oliveira, R.F. and Canario, A.V.M.  “Hormones and social behaviour in cichlid fishes: a case study in the Mozambique tilapia.” Journal of Aquariculture and Aquatic Sciences, Cichlid Research: State of the Art 9 (2001) 187–207.

Romer, U. and Beisenherz W. “Environmental determination of sex in Apistogrammai and two other freshwater fishes.” Journal of Fish Biology.  48.4 (1996) 714-725.

Ser, Jennifer R. et al. “Multiple interacting loci control sex determination in Lake Malawi Cichlid fish.” Evolution. 64.2 (2009) 486-501.

2 Responses to Sexual Differentiation of Cichlids

  1. Peter Canfield says:

    In the section “genetic factors”, you conclude with “Genetic sex can also be overridden by early treatment with exogenous hormones”. Can you elaborate. Further can you provide references for this please.

    • Jung Choi says:

      I’m not the author of this article, but I believe it’s an old fish culture practice to manipulate sex differentiation by adding exogenous steroid hormones to the water. Here’s one reference I found: Hunter, George A., and Edward M. Donaldson. “Hormonal sex control and its application to fish culture.” Fish physiology 9.Part B (1983): 223-303.

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