Hybrid Breakdown

Hybrid breakdown is a decline in viability expressed in the F2 or later linebred generations compared to the F1 or P1. This decline may involve weakness of vegetative growth, sterility, or both of these; it is over and above any loss of vigour due to the lowered heterozygosity of the F2. In its most sudden and extreme form, it causes inviablity of progeny at an early postzygotic stage - from the plant breeders' viewpoint, this is perceived as sterility or lowered fertility in the previous generation. Hybrid breakdown is also known, perhaps more appropriately, as advanced generation breakdown or later generation breakdown.

For example, in many outbreeding perennials which have been hybridised to produce garden cultivars, such as Iris and Watsonia, F2 plants are weaker than their F1 parents but are not sterile. Hybrid cultivars that were derived from the same parent species generally produce weak progeny when intercrossed; but exceptions to this rule occur.

It has been widely recognised that in many interspecies crosses, the viable plants out of the F2 generation tend to resemble either the F1 or one of the original parent species (Levin, 1979). This could be partly due to restrictions on recombination when gametes are formed in the F1, but can be more generally explained by the low viability of many non-parental gene combinations. Harland (1936) hypothesised that the major differences between species are due to differences in 'genetic architecture'. Each has an internally balanced set of genetic modifiers that result in the development of a phenotype that is viable within the habitat to which the species is adapted. Confirming this, in backcrosses of Gossypium hybrids with one of the parent species, there was selective elimination of genes from the other parent at the gametic stage (Stephenson, 1949). Hybrid breakdown could then be attributed to disharmonious actions between certain new combinations of the genes derived from the parent species.

Alleles at different loci that have no effect on fitness singly but combine to cause deleterious or even lethal effects may persist and accumulate in a population, sheltered from selection (Fisher, 1935). One of a pair of such alleles may become common in one population, the other member in another population. When these populations are crossed, segregation will produce individuals homozygous for both deleterious alleles and consequently with lowered fitness. This segregation will occur in the F2 generation if the alleles are unlinked, or in later generations if they are linked and crossing-over is necessary to bring incompatible alleles together.

Such alleles have been called complementary lethals (Oka, 1957), synthetic deleterious loci (Phillips & Johnson, 1998) or complementary genes (Orr, 1995). Such incompatibilities between alleles at complementary loci are likely to be more severe where both loci are homozygous for the incompatible alleles, as in an F2 or backcross, than in the F1 where they are heterozygous. This is again supported by the correlation between distance of relationship and the loss of fertility in F2 hybrids (Gustafsson, 1973).

Since this explanation of hybrid breakdown by complementary genes was stated by Muller (1940), much more evidence accumulated that hybrid breakdown is widespread and due to multiple genes (Levin, 1978). However, the precise details have still been worked out in only a few cases.

It is possible for a viable genotype to arise by selection from among many others of low viability, through many generations of line breeding from an original species cross as demonstrated in Gilia by Grant (1966) and in Helianthus by Riesberg (1997). A population of plants with this genotype is in effect a newly formed species with its own balanced genetic architecture.

Hybrid breakdown has been investigated in most detail in rice. Li et al. (1997) differentiated hybrid sterility from hybrid breakdown, and considered the latter to be caused by incompatibilities between parental alleles at many unlinked loci that cumulatively affect plant vigour. On the other hand, a specific case of hybrid breakdown between cultivars representing the two cultivar groups - Japonica and Indica - of rice is wholly attributable to two unlinked loci (Okuno, 1999; Kubo & Yoshimura, 2002). In this case, only those F2 individuals that have become homozygous for the recessive allele at both loci manifest the symptoms of breakdown: poor growth and sterility.

Other instances of hybrid breakdown in plants may also be due to incompatible alleles at a limited number of loci. This theoretical explanation leads to the following predictions:

• Incompatible dominant alleles will cause weakness in the F1 seedlings, or low seed set in the P1 generation.

• Incompatible non-linked recessive alleles will cause weakness in the F2 seedlings, or low seed set in the F1.

• Incompatible linked recessive alleles will cause weakness in the F3 seedlings, or low seed set in the F2.

• The more loci are involved, the higher the proportion of weak progeny or the lower the seed set.

• Selection over many generations in a hybrid group may remove the alleles that cause hybrid breakdown.

Hybrid breakdown is quite distinct from the phenomenon of inbreeding depression. However, they are related in that both are apparently due to recessive alleles that have negative effects on vigour but are masked in heterozygotes by the positive effects of dominants at other loci.

References

Fisher, R.A. (1935) The sheltering of lethals. Amer. Nat. 69: 446-455.

Grant, V. (1966) The origin of a new species of Gilia in a hybridization experiment. Genetics 54: 1189-1199.

Gustafsson, M. (1973) Evolutionary trends in the Atriplex triangularis group of Scandinavia. I. Hybrid sterility and chromosomal differentiation. Bot. Not. 126: 345-392.

Harland, S.C. (1936) The genetical conception of the species. Biol. Rev. 11:83-112.

Kubo, T. & Yoshimura, A. (2002) Genetic basis of hybrid breakdown in a Japonica/Indica cross of rice Oryza sativa L. Theor. Appl. Genet. 105: 906-911.

Levin, D.A. (1978) The origin of isolating mechanisms in flowering plants. Evolutionary Biol. 11: 185-317.

Levin, D.A. (1979) Hybridization: An Evolutionary Perspective. Benchmark Papers in Genetics 11. (Dowden, Hutchinson & Ross: Stroudsburg).

Li, Z.K.; Pinson, S.R.M.; Paterson, A.H.; Park, W.D. & Stansel, J.W. (1997) Genetics of hybrid sterility and hybrid breakdown in an intersubspecific rice (Oryza sativa L.). Genetics 145: 1139-1148.

Muller, H.J. (1940) Bearing of the Drosophila work on systematics. In Huxley, J. (ed) The New Systematics. (Clarendon: Oxford). 185-268.

Oka, H.I. (1957) Phylogenetic differentiation of cultivated rice, XV. Complementary lethal genes in rice. Japan. J. Genet. 32: 83-87.

Okuno, K. (1999) Geographical distribution of genes causing hybrid breakdown in varietal crosses of Asian cultivated rice. Genetic Resources and Crop Evolution 46: 13-17.

Orr, H.A. (1995) The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.

Phillips, P.C. & Johnson, N.A. (1998) The population genetics of synthetic lethals. Genetics 150: 449-458.

Rieseberg, L.H. (1997) Hybrid origins of plant species. Ann. Rev. Ecol. Syst. 28: 359-389.

Stephenson, S.G. (1949) The cytogenetics of speciation in Gossypium 1. Selective elimination of the donor parent genotype in interspecific backcrosses. Genetics 34: 627-637.

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