Nature 70:186 August 16, 1952
Heterozygosity, Environmental Variation and Heterosis
Forbes W. Robertson
E. C. R. Reeve

Institute of Animal Genetics, Edinburgh

 

1Reeve, E. C. R., and Robertson, Forbes W.,
J. Genet. 51:267-316 (1953)

When a wild strain of Drosophila melanogaster is inbred under optimum conditions, the phenotypic variance of body-size is reduced by not much more than 50 per cent.1 This suggests that nearly half the variance of the original strain was due to the effects of uncontrollable environmental variations within the culture. But highly inbred lines tend to have a much higher variance than crosses between them, so that the environmental variance in such quantitative characters is not constant for all genotypes and tends to be smaller in heterozygotes than homozygotes. This is illustrated in Table 1 for six highly inbred lines and the crosses between them. The lines came from two unrelated wild stocks. Nettlebed and Edinburgh, and include two lines selected for long wings (LN and LE), two selected for short wings (SN and SE) and two unselected lines (UN and UE). Wing-length is closely correlated with body-size, and variance is expressed as squared coefficient of variation, since this measure eliminates most of the effect of differences in absolute size.

Table 1. Phenotypic Variance in Inbred Lines and Crosses
Variance of wing-length in squared coefficients of variation
Strains crossed Parental average F1
LN x SN
LE x SE
UN x UE
SN x UN
SE x UE
SN x SE

Average
1.79
1.44
2.27
2.85
1.78
4.00
——
2.35
  1.37 females only
  0.52 males only
  1.11 sexes combined
  1.88 "
  0.55 "
  2.00 "
  ——
  1.24

The inbred lines have, on the average, almost double the phenotypic variance of the crosses between them, and the tendency is shown by crosses involving large, small and unselected lines. There are probably also differences in variance between the different inbred lines; but part of the differences must be attributed to environmental differences between the experiments in which they were tested.

The relation between heterozygosity and environmental variance has been further analyzed by preparing genotypes containing specific combinations of the three major chromosomes from inbred lines SE and UE, using methods which will be described elsewhere. If these genotypes are grouped according to the numbers of heterozygous pairs of chromosomes they carry, we find that the average variance of wing-length declines progressively with increase of heterozygosity (Table 2), so that the environmental variance of a particular genotype appears to be intimately related to the degree of heterozygosity.

Table 2. Variance and Heterozygosity in SE/UE Genotype
No. of major chromosome
pairs heterozygous
No. of genotypes tested Average variance
of wing-length
Females
0
1
2
3

5
9
5
1

2.54
2.23
1.44
1.20
Males
0
1
2

5
7
2

1.64
1.31
1.19

A partial analysis of the SN x UN cross by the same technique shows the same general trend for size, and in view of the differences in variance between inbred lines and their crosses, it is likely to be a general phenomenon. The same general relationship also appears to hold for rate of egg production, both in comparisons between inbred lines and their crosses, and in comparisons between the specific genotypes of differing heterozygosity referred to above. But problems of scaling make interpretation of these figure difficult, since the heterozygotes tend to have a much greater output than homozygotes. It seems probable that many quantitative characters in different animals and plants will show the same tendency for environmental variability, under given conditions to decrease as heterozygosity increases. It is not to be expected, of course, that the same rule would hold good when one is dealing with individual genes with large effects.

Size in Drosophila shows the same phenomena of decline under inbreeding and heterosis in crosses between inbred lines as other qualitative characters. This suggests that heterosis, or increased size, vigour, etc., and reduced susceptibility to environmental variations are both manifestations of the same phenomenon of heterozygosity. There may be a general explanation for this relationship: the more heterozygous individuals will carry a greater diversity of alleles, and these are likely to endow them with a greater biochemical versatility in development. This will lead to heterosis, because of the more efficient use of the materials available in the environment, and also to a reduced sensitivity to environmental variations, since there will be more ways of overcoming the obstacles which such variations put in the way of normal development.