Nondisjunction in canaries: data of Durham (1926)

Abstract

The largest controlled breeding experiment with canaries, conducted 70 years ago under the auspices of William Bateson (F. M. Durham and D. C. E. Marryat, 1908. Royal Society of London, Reports to the Evolution Committee, Report 4: 57–60.), involved 1300 birds with either black or pink eye color. The difference is governed by two alleles at the Z-linked cinnamon locus. Crosses between pink-eyed males (bb) and black-eyed females (BW) produced unexpected pink sons and black daughters that are attributed to primary nondisjunction in meiosis II of spermatogenesis. Several interdependent estimates of the incidence of nondisjunction progeny range up to 16 ± 3%. Cytological evidence is lacking for Durham's (F. M. Durham. 1926. J. Get. 17: 19–32.) and other presumptive nondisjunction cases in the contemporary literature comprising canaries, doves, and pigeons.

Sex determination in birds: progeny of nondisjunction canaries of Durham (1926)

“…In contrast to the ability of exceptional black females to reproduce, most exceptional pink males that hatched in the stocks of Durham and of contemporary canary breeders failed to mature. It seems reasonable to extend this reduction in post-hatch viability to earlier stages and to regard ZZW canaries as sublethal (Sittmann, 1983). Furthermore, sex ratios between 39-7 % and 447 % in Durham's three main mating types were interpreted to be due to a reduction in viability of ZZZ males as well (Sittmann, 1983).…”

“…Second, the incidence of sex-chromosome aneuploidy was substantially lower in the 16-hour chick embryos (8/2107 = 0-4 %) than in the hatched canaries (23/450 = 5-1 % ; x 2 i = 69-8) where, in addition, the incidence of 51 % is biased down for two reasons. Among trisomic males, at least one class (ZZW, pink) suffered heavy pre-hatch mortality (~ 90% ; Sittmann, 1983) and the other (ZZZ, black) was undetectable among normal (ZZ) black males. In 4-day chick embryos, furthermore, Bloom (1972) found aneuploidy for any macrochromosome in only 9/4182 = 0*2%, all single or double trisomics.…”

“…It seems reasonable to extend this reduction in post-hatch viability to earlier stages and to regard ZZW canaries as sublethal (Sittmann, 1983). Furthermore, sex ratios between 39-7 % and 447 % in Durham's three main mating types were interpreted to be due to a reduction in viability of ZZZ males as well (Sittmann, 1983). For Crew's data (Table 3), the assumption of sublethality of trisomics would reduce the expectation of sons in favour of daughters, thus raising the x 2 f°r 5-5 % nondisjunction.…”

“…Unlike Crew's data, those of Durham have been ignored for over 50 years (Sittmann, 1983). They involve 1300 canaries from controlled breeding experiments conducted before 1910 at Cambridge and then till 1915 at the John Innes Horticultural Institution after Bateson had become its first director.…”

“…Other than primary nondisjunction in meiosis II of spermatogenesis (H B ) or in meiosis I of oogenesis (// D ), no single plausible mechanism (e.g. misclassification, sex reversal, triploidy, partial sex-linkage, secondary nondisjunction, stock-keeping errors) can simultaneously account for exceptional progeny of both mating types (Sittmann, 1983). (Nondisjunction in male meiosis I or in female meiosis II fails for the pink sons in Bb $ x B ?…”