Sex-Linkage of the Black Caudal-Peduncle and Red Tail Genes in the Tuxedo Strain of the Guppy, Poecilia reticulata

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

The authors write..."Two color patterns of the Tuxedo guppy strain, namely, black caudal-peduncle and red tail, were genetically investigated in this study. The loci for the black caudal-peduncle and red tail genes on the sex chromosomes are proposed to be Bcp and Rdt, respectively. Genetic map distances of these genes from the sex-determining region were determined from recombination rates. Our study forms part of an on-going effort to link color pattern genes to the X- and Y-chromosomes and autosomes of the guppy using phenotypic markers"

Description of the fish (by th eauthors)

"Adult males and females of the TUX strain have a total length of 3–4 cm and 5–6 cm, respectively. Adult TUX males have black (melanic) or dark grey pigmentation on the caudal-peduncle region which masks normal wild-type male body coloration, and a caudal fin that ranges from blood-red to orange-red in color (Fig. 1A). Some TUX males may have a metallic blue or green sheen overlying the black caudal-peduncle. TUX females show drab wild-type olive-brown body coloration and grey caudal-peduncle with red tinges of varying intensity on an opaque greyish-white tail (Fig. 1B). Wild-type guppies are smaller than the domesticated TUX strain. Adult WT males are 2–2.5 cm in length and 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 are devoid of color patterns (Fig. 1D )."

Fig. 1. (A) Adult male guppy of the Tuxedo (TUX) strain showing black caudal-peduncle and red tail color patterns. (B) Adult female guppy of the Tuxedo strain with grey caudal-peduncle and faint red tinges on an opaque greyish-white tail. (C) Adult male feral guppy with typical wild-type (WT) male body coloration. (D) Adult female wild-type guppy with a drab olive-brown body that is devoid of any bright color patterns.

Reciprocal crosses

"Inheritance of the black caudal-peduncle and red tail color patterns was elucidated by single-pair reciprocal crosses between the TUX 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: TUX×WT(Table 1A) and WT×TUX(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). All F1 and F2 progenies were segregated and scored according to phenotypes and sex. Progenies displaying color patterns such as Tuxedo, red tail and black caudalpeduncle were designated as the TUX, RT and BCP phenotypes, respectively, and those without such color patterns, WT phenotype. Tuxedo males of parental crosses were typed using Roman numerals (I, II, III, IV and V) according to their putative alleles following segregation of their F1 and F2 progenies. This was to facilitate description of the crosses."

Segregation and recombination in TUX ×WT F1 and F2 offspring

F1 males exhibited the black caudal-peduncle and red tail color patterns of their TUX male parents (Fig. 1E), while F1 females had a grey caudal-peduncle and an opaque greyish-white tail (Fig. 1F).

F1 males and females could have inherited the black caudal-peduncle and red tail color genes only from their TUX male parents (designated as type I). Table 1A also shows three other crosses in which the TUX male parents were heterozygous for black caudal-peduncle and red tail. To facilitate description of these crosses and their offspring, these TUX males were labelled as types III, IV and V. Type II TUX males were not observed in this study although they were found among crosses between the Tuxedo and Green Variegated guppy strains that we carried out in a later study (Khoo et al., submitted). For type III, five mating pairs gave 18 broods of 116 red tail (RT) males and 130 TUX females (Fig. 1E, F, Table 1A). Four F1 broods of 33 WT males and 35 TUX females were produced by the cross between a type IV TUX male and a WT female (mating pair PT1), while 25 BCP males and 29 TUX females were obtained from mating pair PT6 (type V TUX male) (Fig. 1E, F, Table 1A). For all four types (I, III, IV and V) of TUX male parents, the F1 male to female ratio was consistent with the expected ratio of 1:1 (Table 1A)."

F1 and F2 data for TUX ×WT showed that the dominantly expressed black caudal-peduncle and red tail color patterns are due to single genes that are found at two different loci, Bcp and Rdt, respectively, on the sex chromosomes.

Inheritance of the black caudal-peduncle and red tail color patterns

"Observations for all parental (TUX ×WT and WT × TUX) and full-sib (F1 ×F1) crosses indicate that the black caudal-peduncle ( Bcp) and red tail ( Rdt) color pattern genes are responsible for the Tuxedo phenotype of the guppy. This study demonstrates that these two color patterns are simple sex-linked traitscontrolled by single genes: the Bcp allele is dominant for black caudal-peduncle over Bcp+, and Rdt is dominant for red tail over Rdt+. Wild-type or feral guppies do not display these color patterns as they have the recessive Bcp+ and Rdt+ genes (Fig. 1C, D). Using Tuxedo males that were heterozygous for Bcp and Rdt, we have also shown that the expression of Bcp and Rdt is dominant in both males and females (Figs. 1, 2)."

Conclusion

Authors write... "In conclusion, the black caudal-peduncle ( Bcp) and red tail ( Rdt) genes of the domesticated Tuxedo guppy strain (1) occur as single genes at two different loci, and are (2) dominantly expressed, (3) X- and Y-linked, and (4) fully capable of crossing-over from the Y- to the X-chromosome and vice versa since they are situated in an undifferentiated homologous region on these chromosomes.

... "Genetic map distances for the sex-determining region (SdR)– Rdt, SdR– Bcp and Rdt–Bcp are estimated to be 3.4, 5.1 and 2.4 map units, respectively. We therefore propose a phenotypic map of SdR– Rdt–Bcp (Fig. 3) for the Y-chromosome of the guppy. The Bcp and Rdt loci are also inferred to be at similar positions on the X-chromosome that was postulated by Winge (1927, 1934) to have a corresponding feminine segment of the SdR (Fig. 3)."