on chromosome arm 3L (QTL-3L), which both influence the number and length of the internodes in both the primary lateral branch and the inflores- cence (Doebley et al., 1995; Lukens and Doebley, 1999). Alleles at these loci derived from either maize or teosinte had the strongest phenotypic effect in their own species background, further signalling the complexity of genomic interactions in Zea mays. QTL-1L was determined to be the locus for tb1, and QTL-3L could be te1, which we have already described as being highly pleiotropic. Again, selection at these two loci would have had dramatic phe- notypic effects during the domestication process.
barbadense have inrolled leaves, corky stems and bushy growth and are mostly sterile (Stephens, 1946). In some cases, unfavourable gene combina- tions do not appear until the F2generation and more complete reassortment occurs. Crosses of Zauschneria cana Zauschneria septentrionalis (Clausen et al., 1940) and Layia gaillardioides Layia hieracioides (Clausen, 1951) produce vigorous, semifertile hybrids but most of the F2individuals are weak and dwarfish. We shall describe these types of relationships more fully in the chapter on speciation.
Probably the most frequently mentioned case of hybrid breakdown within a plant species involves populations of the bean Phaseolus vulgaris (Gepts, 1988, 1998). There are large- and small-seeded races from South America and Mexico that when crossed produce high percentages of weak, semi-dwarf progeny. This reduction in hybrid fertility and vigour is associ- ated primarily with two independent loci, DL1 and DL2, although many other differences exist in the gene pools of the geographical races, including distinct phaseolin seed proteins, electrophoretic alleles, flowering times and floral structures (Gepts and Bliss, 1985; Shii et al., 1981).
Proper development and function depend not only on nuclear interac- tions but also on nuclear–organelle cooperation. Dramatic differences are found between reciprocal crosses of Epilobium hirsutum and Epilobium luteum (Michaelis, 1954). E. hirsutum E. luteum yields hybrids with stunted growth, narrow yellow-mottled leaves and sterile anthers, while E.
luteum E. hirsutum produces normal-looking plants and fertile anthers.
These differences are presumably the result of the egg providing most of the cytoplasm for the fertilized egg. As with most angiosperms, the egg cell of Epilobiumis rich with organelles, but the sperm cells have little cytoplasm.
Stubbe (1960, 1964) found the plastids of diploid Oenotherain the sec- tion Euoenothera to vary in their functionality in different nuclear back- grounds. He identified five plastome types that differed in their nuclear compatibility (Fig. 3.5). Although the chloroplasts can often survive in the nuclear background of another species, they show varying degrees of bleaching. This dysfunction suggests that the nuclear and plastid genomes coevolved to produce a finely tuned cooperative relationship.
Multigene complexes
There are a number of examples in plants and animals where several genes with related functions are found in close proximity on a chromosome and may represent coadaptation (Ford, 1975). Darlington and Mather (1949) coined the term supergene to describe the case where a series of genes rarely undergo recombination due to tight linkage on a chromosome or association within an inversion. They felt that genes which were originally separate might occasionally migrate together to unify coadapted complexes as selection ‘capitalized’ on cytological aberrations.
Heterostyly in primroses is a clear example of such supergenes (Dowrick, 1956; Crowe, 1964). Successful pollination occurs only between individuals with their stigmata and anthers in the same position (Fig. 3.6) and numerous other characteristics are linked to these traits, including size and ornamentation of pollen grains and the size of stigmatic papillae. Other classic examples of heterostyly are found in the Polygonaceae, Linoceae, Lythraceae, Oxalidaceaeand Boraginaceae(Grant, 1975).
= normal green
= green to greyish green
= yellow green (lutescent)
= periodically lutescent
= yellow green to yellow
= white or yellow
= white and with inhibition of growth and germination
= lethal; but white if occurring as an exception
= slightly yellowing
= periodically pale (diversivirescent)
= periodically pale (virescent)
Plastome
Genome
AA AB BB BC CC AC
Fig. 3.5. Compatibility between different diploid Oenotheranuclear and plastid genomes. Small symbols represent a less frequent occurrence in the A genomes.
(From Stubbe, 1964.)
Fig. 3.6. Relative positions of the stigma and anthers in pin and thrum flowers of the primrose. (From P.W. Hedrick, © 1983, Genetics of Populations, Jones and Bartlett Publishers, Boston, Figure 5.3, p.173. Reprinted with permission.)
The speltoid mutant in hexaploid wheat is another example of a super- gene in higher plants that may even represent a reversion to primitive charac- teristics. The cultivated bread wheat Triticum aestivumnormally has a tough rachis (main fruiting axis) with loose glumes (bracts) that allow the grain to fall out easily. The speltoid mutant mimics the primitive wheat Triticum spelta, in which the rachis is brittle and the glumes are tightly attached. Triticum aes- tivum yields mostly naked seeds when harvested, while the rachides of the speltoid mutants shatter and the seeds remain attached (Frankel and Munday, 1962). The genes involved in this syndrome of traits are clustered together on one chromosome (IX) and all speltoid mutants have a deficiency for a seg- ment called Q (Sears, 1944; MacKey, 1954).
Chromosomal inversion heterozygosities have also been used to argue for coadaptation. Probably the most complete story has been developed in the fruit fly Drosophila (Dobzhansky and Pavlovsky, 1953; Vetukhiv, 1956).
Numerous chromosomal arrangements exist in natural populations of this genus and many of these chromosomal types are maintained in relatively sta- ble frequencies. Dobzhansky and Pavlovsky suggested that these polymor- phisms represented coadapted blocks of well integrated genes and that the most fit individuals were those heterozygous for chromosomal rearrange- ments. They tested their hypothesis by comparing the fitness of homozygous and heterozygous genotypes of Drosophila willistoniand Drosophila pseudob- scura from different localities. When experimental populations were initiated with individuals heterozygous for two inversions, high frequencies of inversion heterozygotes were maintained if the populations were begun with individuals from the same locality, but frequencies of inversion heterozygotes diminished in populations initiated with strains of different localities. They suggested that the genes in the inversions from similar populations were well integrated, while those from distinct populations were not. The gross structure of the chromoso- mal arrangements found in two populations may have been similar, but the alleles they carried were different. This divergence in allelic frequency was later documented by Prakash and Lewontin (1968, 1971) using allozymes.
Such dramatic examples of inversion polymorphism are unusual in plants, but the maintenance of translocation heterozygotes in species like Oenothera are thought to reflect coadapted complexes (Chapter 1). Permanent transloca- tion heterozygotes are maintained through a system of balanced lethals where homozygotes are either weak or not produced due to gametic unviabilities. For example, in Oenothera lamarchiana the chromosomes form a ring of 14 at meiosis and are oriented in such a way that alternate chromosomes pass to each pole (Fig. 3.7). This results in only two types of gametes being produced, one with chromosomes from only the pollen parent and one with chromo- somes from only the mother. A system of balanced lethals then operates in Oenothera to allow only heterozygous zygotes to survive. In one case, only one set of chromosomes produces viable pollen and one set viable eggs (gametophytic lethals), while, in other instances, both types of gametes are formed, but only heterozygous zygotes survive (zygotic lethals).
It is generally agreed that this complex system of structural hybridity could have arisen as a mechanism to preserve coadapted complexes. To test this possibility, Levy and colleagues examined electrophoretic variation among chromosomal complexes of several Oenotheraspecies which carried the gametophytic lethal system (Levy and Levin, 1975; Levy et al., 1975;
Levy and Winternheimer, 1977). He discovered that the species had very few alleles at individual polymorphic loci, but that individual strains had unique combinations of the whole allelic array. The egg and sperm lines of
A B
A
B AB
A B
A
B AB BB
AA AB
Fig. 3.7. System of balanced lethals in Oenothera. (a) Stylized diagram of
chromosome segregation in O. lamarchiana. The chromosomes form a ring of 14 at meiosis, oriented in such a way that alternate chromosomes pass to each pole.
Only two types of gametes are produced, one with all its chromosomes derived from the pollen parent, and the other with a full set from the mother. (b) Two types of balanced lethal systems found in Oenothera where only heterozygous zygotes result. Top, gametophytic lethals where only one chromosome set produces viable eggs and pollen. Bottom, zygotic lethals where both types of gametes are formed, but only heterozygous ones survive. The slashes represent mortality or death. (Used with permission from T. Dobzhansky, F.J. Ayala, G.L. Stebbins and J.W. Valentine,
© 1977, Evolution, W.H. Freeman and Company, San Francisco.)
most strains differed significantly in allelic frequencies at a number of loci and intergenomic linkage disequilibrium accounted for 97.5% of the observed heterozygosity. Thus, particular genic arrays were indeed being maintained in each population – an observation at least consistent with the coadaptation hypothesis.
Gametic disequilibria
In electrophoretic examinations of plant and animal populations, alleles at groups of linked and unlinked genes are often found to be out of Hardy–Weinberg equilibrium. The non-random association of alleles at dif- ferent loci in gametes is referred to as gametic phase disequilibrium or the shortened form, gametic disequilibrium (Lewontin and Kojima, 1960; Crow and Kimura, 1970).
As we have already noted, genetic analyses involving multiple loci are quite complex. To measure gametic phase disequilibria, the frequencies of all possible allelic combinations are calculated and then compared with each other. Excesses of one gametic type that do not equilibrate after several gen- erations of mating are thought by many population biologists to represent coadapted complexes.
For example, using the simplest case of two loci with the alleles Aa and Bb:
Gametes carrying AB and ab are said to be coupling gametes.
Gametes carrying Ab and aB are said to be repulsion gametes.
Gametic phase disequilibrium (D) = product of coupling genotype fre- quencies product of repulsion genotype frequencies
Mathematically, if:
Locus 1 Locus 2 A = p1 B = p2 a = q1 b = q2 then:
D = (p1p2)(q1q2)(p1q2)(q1p2) and to weight by gene frequency:
D= D/pq
= relative gametic phase disequilibrium Dvaries from +1 to 1, and:
if D= 0, there is no disequilibrium
if Dis negative, there are more repulsion than coupling gametes if Dis positive, there are more coupling than repulsion gametes
Populations with positive and negative values of D have a surplus of one or the other gametic type and are therefore in gametic phase disequilibrium.
This means that alleles at each of the loci are not segregating independently and distinct genic assemblages are being maintained.
The most commonly cited examples of gametic phase disequilibria in plants are those of Allard and his co-workers (Allard et al., 1972; Allard, 1988), although others have been documented (Golenberg, 1989). We described pre- viously the association between allelic frequencies at single loci and moisture levels in oats (Chapter 2). These alleles were further clustered into a few non- random associations across loci. The mesic environments were almost monomorphic for a set of alleles at five loci (denoted 21112), while on the more xeric sites only two sets of alleles predominated (12221, 12211) (Table 3.1). Three of these loci were on the same chromosome, while the other two segregated independently (Clegg et al., 1972). When the Dvalues were aver- aged across all of the possible two-locus pairings, values ranged from 0.36 to 0.71 in each of the various subdivisions. The direct adaptive benefit of these alleles was not measured, but the most common assemblages were thought to represent coadapted complexes since they were not in the expected frequencies.
Allard and co-workers (Clegg et al., 1972; Weir et al., 1972) also found associations between alleles at different electrophoretic loci in cultivated populations of barley (Hordeum vulgare). They examined seed samples of two highly heterozygous experimental populations (CCII and CCV), which were initially generated by hybridizing 30 parents from the major barley pro- duction regions of the world. These populations were propagated in large plots under agricultural conditions for decades without conscious human- directed selection. It was discovered that some allelic combinations had Table 3.1. Changes in five-locus gametic percentages in wild oats along a moisture gradient. Subdivisions A, B, C and D represent a change from mesic to xeric conditions.
(From Allard et al., 1972.)
Gametic Subdivision
Location
typea A B C D total
21112 91.5 39.9 16.9 1.9 56.7
12221 1.7 4.1 27.9 31.9 11.3
12211 0.1 1.5 3.2 30.5 4.0
11112 0.7 4.8 2.7 0.6 1.8
21121 0.7 5.8 8.8 5.7 4.0
21221 0.0 4.6 5.6 1.6 2.2
12212 0.4 10.7 1.5 0.3 2.2
22221 0.2 3.9 6.5 2.0 2.5
D 0.71 0.36 0.52 0.39 0.64
aTwo alleles (1 and 2) at five loci – esterase loci E4, E9, E10, phosphatase locus P5and anodal peroxidase locus APX5.
increased over time, while others had declined (Table 3.2). The Allard group hypothesized that natural selection was structuring ‘the genetic resources of these populations into sets of highly interacting, coadapted gene complexes’.
While these gametic disequilibria could indeed be the result of coadap- tation, the possibility cannot be excluded that the changes are the result of the ‘hitchhiking’ of allozyme loci with other major adaptive genes (Hedrick and Holden, 1979; Hedrick, 1980). The loci examined by the Allard group may be selectively neutral but linked to other genes that are selectively important. Since both oats and barley are highly selfed, gametic disequilibria could arise without strong epistatic interactions.
A similar argument can also be made about the electrophoretic variation observed in the chromosomal inversion types of Drosophilaand Oenothera.
Over time, neutral allozyme loci within the different chromosomal types might have gradually diverged due to random forces, since the chromoso- mal types would be operating as separate gene pools due to the unviability of heterogenetic crossovers (Nei and Li, 1975). Still, the persistence of chro- mosome heterozygosities in natural populations argues that at least some adaptively important genes are found on the variant chromosomal types.
Complex gene interactions in polyploids
Poor performance in selfed autopolyploids is usually attributed to the loss of higher order allelic interactions in what is known as the overdominance
Table 3.2. Most common tri-allelic four-locus gametic types (percentages) found in complex hybrid populations of barley (CCII and CCV) over several generations. Only the most common genotypes are shown. (From Clegg et al., 1972.)
CCII Generation
Gamete 7 18 41
1221 7.1 6.2 5.2
2112 10.9 2.1 49.7
2113 11.5 11.5 24.8
CCV Generation
Gamete 5 17 26
1221 0.9 3.0 17.3
2111 12.9 17.0 17.3
2112 3.8 6.3 8.5
model of inbreeding depression (ID) (Bever and Felber, 1992). Stated in another way, vigour in autopolyploids is positively correlated with the num- ber of different alleles at each locus.
Evidence for the existence of complex interallelic interactions in autopolyploids has come from the observation that inbreeding depression in autopolyploid lucerne (Busbice and Wilsie, 1966; Busbice, 1968) and potato (Mendoza and Haynes, 1974; Mendiburu and Peloquin, 1977) is much greater than would be predicted by the coefficient of inbreeding in a two- allele model. Busbice and Wilsie (1966) suggested that this rapid loss of vigour is associated with the theoretical rate at which loci with three and four alleles are lost (tri- and tetra-allelic loci). Correlative data have come from comparisons of autotetraploids with different genetic structures. Bingham and his group (Dunbier and Bingham, 1975; Bingham, 1980) produced diploids from natural tetraploids by haploidy, generated diploid hybrids and then doubled the diploid hybrids using colchicine treatments to obtain defined two-allele duplexes (di-allelic loci). These were then crossed to pro- duce double hybrids with presumed tetra-allelic interactions. When the per- formance of these different structured populations was compared,
‘progressive heterosis’ was observed as the diploid hybrids had higher herbage yield (540 g/plant) than their diploid parents (237 g/plant), and the double hybrids had the highest yield of all (684 g/plant).