(This article was originally published in Cichlid News Magazine Jul-97 pp. 20-21, it is reproduced here with permission from Ronald Coleman and Aquatic promotions).
In the Midas cichlids, Amphilophus citrinellus, adult males are typically larger than females. Photo by Ronald Coleman.
When selecting Neotropical (or other) cichlids, experienced breeders usually choose equal numbers of large and small individuals to be sure of getting both males and females. It has long been known that the largest fish in a brood would turn out to be males, while the smallest would end up as females. Why is that?
The most reasonable explanation for this phenomenon has always been that males grow faster than females. But, as with so many things about cichlids, just because something is reasonable doesn't mean it is true. A simple, yet elegant experiment by Richard Francis and George Barlow (University of California at Berkeley) revealed that for at least some cichlids, it is not sex that determines size. Rather it is the other way around: size determines sex.
As bizarre as it sounds, some individuals become males because they are growing faster and becoming larger than their siblings, while the smaller individuals mature as females. This remarkable flexibility is only possible because sex isn't determined in cichlids the same way it is in humans.
In mammals (including humans), sex determination is all in the genes. A female human has two X chromosomes, while a male has an X and a Y. As such, the mother always contributes an X to each offspring, while the father has a 50% chance of contributing an X and a 50% chance of contributing a Y. The sex of each offspring is entirely determined by which chromosome the father contributes. Birds are the opposite: it is the females that have two different sex chromosomes while the males have two of the same.
Fish do things differently, and as befits the diversity of fishes, there is diversity in how sex is determined. If you were to peek inside the cell of a male mammal using high magnification you could actually see the X and Y chromosomes. They look different. This is seldom true in fishes; instead the sex chromosomes usually look the same. While in some fishes there appears to be chromosomal inheritance of sex, often sex determination is more flexible, influenced by environmental factors such as temperature, pH, hormones, and social conditions. Even in cases where there is chromosomal inheritance of sex, extreme treatments can "override" the genetic basis of sex. For example, genetically female guppies will mature as males if raised in extreme temperatures (Francis, 1992). Recent work on cichlids is revealing the extent of this flexibility.
David Rubin (1985) of Clark University followed up on Heiligenberg's (1965) observations that sex ratio in broods of Pelvicachromis ("kribensis" and relatives) seemed to vary with pH. Rubin bred pairs of P. pulcher, P. taeniatus, and P. subocellatus and raised the offspring at various pH levels. He determined their sex around 180 days after hatching either by dissection or by external observations. The results agreed with Heiligenberg: acid water tended to produce more males and basic water gave more females. For example, at a pH of 5.0, 96% of a P. pulcher brood became males, while at a pH of 6.9, only 20% became males. He obtained similar results for the other two "krib" species. Rubin also experimented with two species of Apistogramma (A. borellii and A. cacatuoides) and found the same thing.
Very recently, Uwe Romer and W. Beisenherz (1966) examined sex determination in 37 species of Apistogramma. They created pH treatments of 4.5, 5.5, and 6.5, and temperature treatments of 23, 26, and 29°C. They found that in some species (e.g., A. cacatuoides, A. gephyra, A. hongsloi, A. nijsseni, and possibly A. steindachneri and A. linkei), pH influenced sex ratio, low pH favoring the production of males. Interestingly, they found that higher temperatures also produced more males, this time in 33 of 37 species examined; the only exceptions were A. iniridae, A. luelingi, A. mendezi, and A. sp. "Gelbwangen," and even in those cases the results were almost significant. The effects of temperature and pH were not "all-or-none," i.e., not even high temperature and low pH together produced 100% males; rather, all broods contained a mix of the sexes, but the mixture changed according to temperature, pH, and species. The greatest skews were 99% males in A. diplotaenia at pH 4.5 and 29°C versus 4% males in A. caetei at ph 6.5 and 23°C In Pseudocrenilabrus multicolor victoriae (the only African cichlid they investigated), neither temperature nor pH influenced sex.
It was in light of this extraordinary flexibility that Francis and Barlow conducted their experiment. They used the Midas cichlid, Amphilophus citrinellum, from Central America. Midas cichlids are large, substrate-spawning, biparental cichlids common to the Great Lakes of Nicaragua. Adult males can easily reach 25 cetimeters in length, and females grow a bit smaller. A typical spawn from an adult female may comprise 2000-3000 eggs.
Francis and Barlow started with a brood of Midas cichlid fry and raised them together for six months. At the end of this time they sampled 74 juveniles from this group which they carefully measured. The median standard length was 52.2 mm (roughly 2"). The researchers then took the 37 fish larger than the median and put them in their own tank and called it the "Large" group. They put the 37 fish smaller than the median together in a different, but identical, enclosure designated the "Small" group. The fish were then allowed to grow and mature for another six months.
Even at three months of age, fry from a single brood of Midas cichlids can vary greatly in size. Photo by Ron Coleman.
From their size at the initial measuring, we would expect the bulk of the fish in the "Large" group to mature into males, while the bulk of the "Small" fish should mature into females. However, when Francis and Barlow looked at the fish at one year of age, that is not what they found. At one year the fish were starting to mature sexually and by examining the fish externally (and then confirming the observations by dissections), the researchers found that roughly half the fish in each enclosure were male, and half were female. Furthermore the large fish in each enclosure were the males, and the smaller ones were the females. In the "Large" group, males ranged from 116-143 mm SL, while females ranged from 96-123 mm. In the "Small" group, males were 129-155 mm SL, while females were 105-128 mm.
The only explanation for this data is that the largest fish in each enclosure "decided" to become male, while the smaller ones "decided" to become females. The experiment shows that sex determination in these' fish occurred sometime between six months and one year, and roughly between 50 and 100 mm in standard length. The cichlids became one sex or the other not simply based on their absolute size, but rather based on their size in relation to the fish around them. Future experiments are needed to see if this social control of sex is widespread among cichlids. For the hobbyist, the bottom line is that the simple question of determining which are the males and which are the females is not a simple question at all!
- Francis, R. C. 1992. Sexual lability in teleosts: developmental factors. Quart. Rev. Biol. 67:1-18.
- Francis, R. C., and G. W. Barlow. 1993. Social control of primary sex differentiation in the Midas cichlid. Proc. Nat'l. Acad. Sci. USA 90:10673-10675.
- Heiligenberg, W. 1965. Color polymorphism in the males of an African cichlid fish. J. Zool. 146: 95-97.
- Romer, U., and W. Beisenherz. 1996. Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). J. Fish Biol. 48:714-725.
- Rubin, D. A. 1985. Effect of pH on sex ratio in cichlids and a poeciliid (Teleostei). Copeia 1985: 233-235.