The topic of this article may be misleading since it does not deal with determining the gender of a specific fish, whether it is a male or a female, but rather about how gender is developed in cichlids after birth. For us humans (and mammals) the gender of an individual is pretty straightforward since the beginning of our lives, but in fish (and many other organisms) it is not always so. In many cichlids the gender is plastic, and we are getting to learn more and more about this fact.
For a time now it has been known to cichlid specialists that in a given batch of young cichlids those larger fish are males and the smaller are the females. Is it sex that determines size of is it the other way around? Amazingly, at least for a number of species the latter seems to be the case.
This paradox contradicts the experience with our own kind, since humans’ gender is hardcoded in the genome: of the 23 pairs of chromosomes comprising our DNA (one chromosome in each pair obtained from the father and one from the mother). The first 22 pairs of chromosomes are similarly shaped in males and females, the 23rd pair however (known as the sex chromosome) can have two different shapes, a regularly shaped chromosome which we call X and a tiny one which is called Y. Females always have two X chromosomes in the 23rd pair, while males have one X and one Y chromosome.
When passing genetic material to our offspring, each human randomly passes one of each of their 23 pairs of chromosomes (the gamete). Females, having two X chromosomes, pass one on, but males, having one X and one Y chromosome, pass each to half of their offspring. The offspring receiving the Y chromosome become male, and those inheriting the X chromosome from their father are born female. Male humans pass gender to their offspring at time of conception. In fish, sex chromosomes are not evident, and chromosomal sex determination may still be evolving.
In fish, sex is not always inherited and often develops after birth, depending on the specific ecological conditions or the individual physiology of each specimen. For example, Reddon & Hurd (2013) determined that the pH of the water during early development of the African riverine cichlid Pelvicachromis pulcher influences its sex ratio and even the male morph! After close to one year of spawning of captive pairs, they found that fish that had been raised at a pH of 5.5 had produced more males than those raised at a higher pH (6.5). In both cases more females than males were produced, as found under natural conditions. Besides that, they also found that fish raised at a lower pH produced a greater proportion of males of the red opercula phenotype (versus the yellow opercula phenotype) of this species.
The assumption of the authors regarding the latter experiment is that the rainy season may alter the pH of the rivers and streams which P. pulcher naturally inhabits (a range that varies between pH 5.5 and 7). P. pulcher breeds year round and fish born during the rainy season may need different gender and male morph ratios than fish born during the dry season in order to gain evolutionary fitness—presumably due to different challenges encountered during each season.
In relation to temperature, a recent study (Nivelle et al., 2019) shows that in the case of fry (10 to 30 days post fertilization) of Oreochromis niloticus, a change of sex can be induced by manipulating the water temperature, resulting in more males as the temperature goes up. The study also shows that during this developmental phase a short time exposure to high temperatures is sufficient to skew the sex ratio of the fry, and, most interestingly, that some individuals may seek the gender-changing high temperatures during this period. The advantages of such a sex reversal mechanism are, however, unknown.
Römer & Beisenherz (1996) carried out an experiment using 37 species of Apistogramma, a genus of South American dwarf cichlids. In their experiment, the authors exposed each of the studied species to changes not just in temperature but also in pH during early development. They found that in 33 of the Apistogramma species they studied (with the other four in doubt due to the small number of individuals used in the study) high temperatures (around 29 °C) significantly influenced the sex ratio towards males, while at lower temperatures (around 23 °C) towards females. They induced the changes during the first month of fry development. In Apistogramma trifasciata for example, they found that at 23 °C fewer than 20% of the individuals became males, while at 29 °C over 80% did.
They also found that a low pH would cause the same effect in several species. In some species, notably A. caetei, temperatures did not significantly impact the sex ratio, which was, however, strongly influenced by pH. In this particular species and conversely to the other studied, a higher ratio of males was produced at lower temperature. In this species sample, around 50% of the studied individuals became males at a pH of 4.5 while just less than 10% did at a pH of 6.5.
Another interesting result of this study refers to a widely distributed African cichlid species, namely Pseudocrenilabrus victoriae, which they also included, and for which no sex bias was observed at different temperatures or pH—an indication that this particular mechanism does not apply to all cichlid species.
In no instance in the study was the number of males reduced to zero or increased to 100%, which, if sustained, would of course lead to the extinction of the species. The gender shift of developing Apistogramma is an open field of study in which they try to understand the environmental forces that make this gender correlation necessary.
We should consider that for a population of a given species to survive, a specific ratio of males to females has to exist; this ratio has been favored by the environment in maintaining the population stable. If more males than necessary are present, some males may not be able to pass their genes to future generations and hence adults that produce more females will be preferred by natural selection, and the other way around. Deviation of the optimum male to female ratio can just be temporal in order to cope with specific environmental conditions.
Let’s consider the Apistogramma case, which are typically polygynous harem brooders, with larger males holding large territories in which several females may simultaneously brood and raise fry. At first sight it would make little sense, evolutionary seen, to have an equal number of males and females, since many males won’t have a chance to reproduce and pass on their genes. Certainly, in several cichlid species this problem has been reduced by the presence of sneaker males who cheat dominant males and spawn with available females. However, this behavior would hardly resolve the problem since one dominant male may have half a dozen or more females in his territory, available all the time. Under normal environmental conditions a given ratio of one male to several females may be the optimum evolutionary solution, but when there is a surplus of males there is competition between them and only the strongest ones get to pass on their genes.
A very interesting paper by Ross Robertson (1972) sheds light on sex change in fish. The study was carried out observing the behavior of the cleaner wrasse (Labroides dimidiatus) in the Great Barrier Reef. Cleaning stations are formed by one colorful blue male and a harem of three to six mature females. The colorful male dominates the harem and the females have their own hierarchy based on their size. Every evening the male spawns with the dominant female and then with the rest of the females according to the hierarchy level. If the male is removed from the colony, the female in the top position undergoes an amazing metamorphosis, transforming her ovaries into testes and subsequently occupying the male’s position. Since she has the larger size, it is the best chance for a rapid replacement.
Coming back to size as a determination force of gender, one of my favorite experiments involves a Central American cichlid species of the San Juan River basin in Nicaragua and Costa Rica: Amphilophus citrinellus. This species is commonly known as the Midas cichlid due to the regular development of xanthic individuals in the Nicaraguan lakes, that are born gray but turn gold or bright orange as they age. Males of this species can grow to over 25 cm in total length, with females remaining smaller.
The experiment was undertaken by Richard Francis and George Barlow (1993), when out of a batch of immature Midas cichlids that had been raised together for six months (then averaging 5 cm), they selected 74 specimens which they separated in two equally numerous groups, those with smaller fish and those with larger. They assumed that if raised together the larger fish at this point would become all males and the smaller fish all females. After separately raising both groups for another six months, they again separated from each group the smaller and the larger individuals. Upon close examination it turned out that those larger fish in each group were males and those smaller females, half the number in each case. The fish had apparently developed their gender as a result of their relative larger size to their group companions. This determination happened before they reached 10 cm.
One hypothesis that Barlow (2002:62) drew from his experiments is that in growing in close quarters, smaller fish would be subject to more stress than larger ones. The fish under stress produces stress hormones that might be actually influencing the gender of that individual.
The mechanism in which an organism begins life as a female and then changes into a male is known as protogyny, and the first example found in cichlids was Crenicara punctulata, a species in which one male spawns with several smaller females. But what about sex change in adult fish? George Barlow (2002:61) reports that this happened in his lab, both with Sarotherodon melanotheron and Etroplus maculatus. He narrates how after separation breeding pairs of Etroplus maculatus in tanks with just proved males and females (they had previously spawned), he observed that some of the females paired off with other females and that they actually spawned. To his surprise, some of the eggs hatched! Species which exhibit this capacity are known as protogynous (or sequential) hermaphrodites. Later on, Barlow found that the Midas cichlid, Amphilophus citrinellus, though rarely expressed, has this capacity as well.
Once it was known that cichlids can develop their gender as they age, it was found that treatments of small fish with sex hormones could lead to masculinization. This has been widely used for Oreochromis niloticus and other species (including Petenia splendida) for aquaculture purposes. This treatments lead to more colorful, only male fish populations (red in the case of O. niloticus). Males alone grow larger as they do not waste energy in breeding efforts, while the water where they are raised maintains a lower level of metabolic wastes that their growing young would produce (Tuan et al., 1998). Hybridization of two (not closely related) species can also produce fry that is just one gender (, 1982).
A situation related to gender and male proportion is the presence of polymorphic males in some cichlid species, with males that thrive in different ways, including turning into sneakers. One fascinating example of a polymorphic cichlid is that of ‘Lamprologus’ callipterus from Lake Tanganyika (2013), with apparently three different male morphs. The territory guarding male is by far the largest with up to 15 cm in total length, and one of the vertebrates that has the biggest size ratio between male and female—up to 60 times larger than a female. Adult males establish territories in sandy areas close to rocks and collect shells from the surroundings (even stealing them from other males’ territories), which they group in a small area they defend. Each territory can contain a dozen or more females each occupying a shell in the territory. The male fertilizes the eggs, which are deposited inside the female’s shell, from the outside of the shell. A second morph of male is the so-called sneaker male, which is identical in size to a female, and can dash in and steal a fertilization at the slightest distraction of the dominant male, during spawning. A third morph is that of a dwarf male, which remains very small (2–4 cm) and occupies the inside of a shell ahead of the resident female during spawning, being able to fertilize some eggs during spawning in safety. It has been found (Wirtz-Ocaña et al., 2013) that the morph of an adult male is determined by genes inherited from the father (normal or dwarf male), while females have only one morph. I have observed this latter case of male inheritance for different morphs in several Xiphophorus (swordtails) species.
As in other occasions, for more insights about this fascinating topic I recommend reading chapter three of George Barlow’s book, The Cichlid Fishes (Nature's Grand Experiment in Evolution).
- Barlow, George W.. 2002. "The Cichlid Fishes (Nature's Grand Experiment in Evolution)". Perseus Publishing. pp. 352 pp. ISBN: 9780738203768 (crc03927) (abstract)
- Francis, Richard C & G.W. Barlow. 1993. "Social control of primary sex differentiation in the Midas cichlid". Proceedings of the National Academy of Sciences of the United States of America. v. 22, (n. 90), pp. 10673-10675. DOI: 10.1073/pnas.90.22.10673 (crc09318) (abstract)
- Konings, Ad. 2013. "Species profile: exLamprologus callipterus (Boulenger, 1906)". The Cichlid Room Companion. Retrieved on 24-Dec-2020, from: https://cichlidae.com/species.php?id=58 (crc10245) (abstract)
- Lovshin L.L. 1982. "Tilapia hybridization". The biology and culture of Tilapias. v. 7, pp. 279-308 (crc09320)
- Nivelle, Renaud & Vincent Gennotte, Jules Kembolo Emery, Kalala, Nguyen Bich Ngoc, Marc Mullerid, Charles Mé Lard, Rougeot Carole. 2019. "Temperature preference of Nile tilapia (Oreochromis niloticus) juveniles induces spontaneous sex reversal". Plos One. v. 14(n. 2), pp. 1-19. DOI: 10.1371/journal.pone.0212504 (crc09317) (abstract)
- Reddon, Adam R & Peter L Hurd. 2013. "Water pH during early development influences sex ratio and male morph in a West African cichlid fish, Pelvicachromis pulcher". Zoology. v. 116(n. 3), pp. 139-143. DOI: 10.1016/j.zool.2012.11.001 (crc09316) (abstract)
- Römer, Uwe & W. Beisenherz. 1996. "Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei)". Journal of Fish Biology. v. 48, pp. 714–725 (crc05103) (abstract)
- Tuan, P. A & D.C Little & G.C Mair. 1998. "Genotypic effects on comparative growth performance of all male tilapia Oreochomis niloticus (L.)". Aquaculture. v. 159(n. 3-4), pp. 293-302 (crc09319)
- Wirtz-Ocaña, Sabine & D. Schütz, G. Pachler, M.Taborsky. 2013. "Paternal inheritance of growth in fish pursuing alternative reproductive tactics". Ecology and Evolution. v. 3, (n. 6), pp. 1614-1625. DOI: 10.1002/ece3.570 (crc05200) (abstract)
© Copyright 2020 Juan Miguel Artigas Azas, all rights reserved
Artigas Azas, Juan Miguel. (December 24, 2020). "Gender determination in cichlids". Cichlid Room Companion. Retrieved on January 24, 2021, from: https://cichlidae.com/section.php?id=312.