Genetic Basis of the Variegated Tail Pattern in the Guppy, Poecilia reticulata

Gideon Khoo, Tit Meng Lim, Woon-Khiong Chan and Violet P. E. Phang

ZOOLOGICAL SCIENCE 16: 431–437 (1999)

The authors write... "Color patterns on the caudal fin of domesticated guppy strains take the form of single bright colors, snakeskin-like reticulations and variegated mosaic patterns of two or more colors. Recent farm surveys show the popularity of reticulated snakeskin and variegated patterns (approximately 15 and 13 strains, respectively) among guppy strains that are commercially cultured for export. The snakeskin pattern has been found to be caused by two genes, Sst and Ssb (Phang et al., 1989a, b, 1990; Phang and Fernando, 1991), while red, blue and green tail colors are attributed to the Rdt, Blt and Grt genes, respectively (Fernando and Phang, 1989; Phang et al., 1991). The term “variegated” is usually applied in the guppy to an exceedingly variable mosaic pattern of black spots and patches of different shapes and sizes on a brightly colored tail fin. No two male or female offspring, including those of the same parents, have been observed to possess similar variegated patterns. With the exception of the Variabilis gene ( Va) in wildtype guppies, described by Winge (1927) as having considerable phenotypic variation in the number, size and position of red side patches and black specks as well as a labyrinthine caudal fin pattern, there are no other reports on genes that control highly variable body and tail fin patterns in the guppy. Therefore, the main objective of this study was to investigate the genetic basis of the variegated tail pattern and its mode of inheritance in domesticated guppy strains."

Source of the fish
"Three- to four-week old fry of the Green Variegated (GV) guppy strain were obtained from Swee Hing & Brothers Aquarium Co. in Singapore. Wild-type (WT) guppies were collected from an isolated hill-stream near the Bukit Timah nature reserve in Singapore. Juvenile GV were cultured in 180-liter fibreglass tanks (30 fish/tank) in the aquarium area of the Department of Biological Sciences, National University of Singapore, at temperatures of 25–28°C. WT fry were separated from the collected samples and raised in 30-liter clear plastic tanks (20 fish/tank). Under laboratory conditions, sexual maturation of WT fry usually occurs at 4-6 weeks of age. Juvenile WT were checked daily for developing males which is recognised by the formation of the gonopodium from the anal fin. Males, when spotted, were immediately removed and reared separately from females as virgin females were necessary for the reciprocal crosses."

Description of the fish
"Adult males and females of the GV strain have a total length of 3–4 cm and 5–6 cm, respectively. Adult GV males have a green metallic sheen overlying the wild-type male body coloration that comprise small spots or patches of various colors. Only GV males have an orange tail with some yellow streaks, and numerous black spots and patches of different shapes and sizes (Fig. 1A). GV females show wild-type female olive-brown body coloration and faint greyish-brown variegated patterns on a yellowish tail (Fig. 1B). Wild-type guppies are smaller than the domesticated GV strain. Adult WT males are 2– 2.5 cm in length while the females are about 3–4 cm. As described earlier, WT males have highly polymorphic color patterns on the body and fins (Fig. 1C), while WT females totally lack any color patterns (Fig. 1D)."

Reciprocal crosses
"Inheritance of the variegated tail pattern was elucidated by singlepair reciprocal crosses between the GV strain and WT stock, using six-week old mature virgin fish. Each pair was kept in a 3.5-liter breeding tank. Broods were produced 4-6 weeks after mating. Single-pair full-sib F1 males and F1 females were mated to obtain the F2 generation. The following notations were used: GV × WT (Table 1A) and WT × GV (Table 2A) for parental crosses, and F1 × F1 (Tables 1B, 2B) for full-sib F1 crosses. Newly born fry were separated and raised to maturity in 3.5-liter clear plastic tanks (five fish/tank). F1 and F2 progenies were segregated and scored according to phenotypes and sex. All progenies displaying variegated tail patterns were designated as the VAR phenotype and those without such patterns, WT phenotype."

PARENTAL STRAINS (A) Adult male guppy of the Green Variegated strain. (B) Adult female guppy of the Green Variegated strain. (C) Adult male wild-type guppy. (D) Adult female wild-type guppy.

F1s. (first genetation)(E) F1 males showing typical variegated tail patterning (top) and wild-type tail without any patterns (bottom) from mating pair PG9. (F) F1 female with variegated tail patterning.

F2s (second generation). (G) F2 males of the VAR (top) and WT (bottom) phenotypes. (H) F2 females of the VAR (top) and WT (bottom) phenotypes.

In the GV × WT cross, F1 males and females could have inherited the variegated pattern only from the GV male parent. The F2 generation comprised a total of 252 VAR males, 114 VAR females and 103 WT females (Fig. 1G, H) with the observed numbers agreeing with the expected 2:1:1 ratio

The F1 and F2 results gave evidence that the putative genotype typical of GV males is XVarYVar. A genetic model illustrating the segregation of the dominant Var gene is presented in Fig. 2.

Figure 2.
Schematic diagram of the proposed genetic models illustrating the segregation of the Var tail color pattern gene, phenotypes and genotypes of the parents (P), F1 and F2 progenies, and recombinants (R) that occur in reciprocal crosses between the Green Variegated (GV) and wild-type (WT) guppies. Mating pair PG9 in which the GV male parent was heterozygous for the Var gene and its F1 and F2 progenies (indicated as9) are shown within thin borders to distinguish them from the typical GV x WT cross.

The Var gene
"Results of all parental (GV × WT and WT × GV) and full-sib (F1 × F1) crosses indicate that the highly variable variegated tail pattern of the Green Variegated guppy strain is a simple sex-linked trait controlled by a single gene with two alleles, Var dominant for variegated tail pattern over Var+ recessive for wild-type which do not exhibit these patterns (Fig. 2). This is the first study that reports the expression of the variegated tail pattern gene, Var, was dominant in both sexes. Our results also show that the Var allele is able to cross over from the Y- to the X-chromosome and vice versa as male and female recombinants of the WT phenotype were obtained from the F2 progenies of GV× WT and WT× GV, respectively"

CONCLUSION

The variegated tail pattern gene, Var, of domesticated selected guppy strains

(1) shows dominant expression,

(2) is both X- and Y-linked,

(3) fully capable of crossing-over from the Y- to the X-chromosome and vice versa,

(4) located about 1.9 map units from the sex-determining
region.