Argemone mexicana

Argemone platyceras

Hagedoorn and Hagedoorn (1921) note that several strongly aberrant types appeared in the F₂ generation derived from the cross Argemone mexicana × A. platyceras (Mexican pricklypoppy × rough pricklypoppy). Some differed from either parent with respect to characteristics usually considered fundamental with respect to taxonomic classification (such as sepal and carpel number). The reader can see that many of the violet hybrids produced by Brainerd (Figure 2.1) have leaf shapes that are not obviously intermediate between the leaf shapes seen in their parents.

Any trait can be heterotic, but most reports of heterosis involve the overall size of the hybrids. The California redwood (Sequoia sempervirens), thought to be of hybrid origin, is the tallest tree in the world. Therefore, with respect to height, it is certainly not intermediate between its probable parents, the giant sequoia (Sequoiadendron giganteum) and dawn redwood (Metasequoia glyptostroboides).

Hybrids between the Bactrian Camel (Camelus bactrianus) and the Dromedary (C. dromedarius), which are partially fertile in both sexes, have long been bred because they are larger, more tolerant, and easier to work with than either parent. According to Lakoza (1938) "in certain very important camel-breeding regions nearly the entire stock consists of hybrids of various grades." Gray (1972, p. 161) states that these hybrids "show heterosis with regard to body measurements, hardiness, endurance, longevity and certain blood characters." Hybrids between Siberian Crane (Grus leucogeranus) and White-naped Crane (G. vipio) are bigger than either of their parents (Maksudov and Panchenko 2002: 199).

A Liger - Lioness x Tiger Heterosis in a mammalian hybrid (click to enlarge)

Similarly, the hybrid produced by a lion and a tigress (known as a "liger") is usually larger and stronger than either of its parents, whereas the reciprocal cross produces a hybrid (the "tigon") that tends to be smaller than either of its parents (Gray 1972, McCarthy, in prep.). The former cross, then, is an example of positive heterosis, in which the hybrid exceeds the range of variation exhibited by its parents, while the latter is an example of negative heterosis, in which the hybrid falls below the range of parental variation with respect to a given trait.

Nevertheless, the typical hybrid, produced by the typical hybrid cross, is intermediate in size. For this reason, Stebbins (1950: 285), speaking before the advent of modern molecular techniques for the identification of natural hybrids, noted that

the detection of an existing species or subspecies as a new [i.e., as a nonintermediate] derivative of past hybridization is well-nigh impossible, since by definition such new types would not be recognizably intermediate between their parental species.

This factor, then, must surely have contributed to underreporting of nonintermediate natural hybrids.

Heterosis is of particular evolutionary interest because it allows hybridization to produce new traits beyond the range of ordinary parental variation. For example, in Algeria Ophrys murbeckii, an orchid of the Atlas Mountains, is derived from hybridization between O. fusca and O. lutea, but it occurs at higher altitudes than either of its parents.

Johnson and Leefe (1999: 1065) report that the snail Campeloma parthenum (Maiden Campeloma) has a five-fold greater survival rate under stressful conditions than one of the parents that crossed to produce it, C. geniculum (Ovate Campeloma).

Grant and Grant (1996b) showed hybrid Galapagos finches (genus Geospiza) were more fit than their parents following an El Niño climatic perturbation event; the hybrids were better able to feed on the seeds of the plants present after the event.

In some crosses, the hybrids produced are actually more viable and vigorous than either parental type. For example, Rockwell et al. (1961) say

It is especially in their larger tolerances that the newer [hybrid] strains of garden lilies show their merits. Through selection of the sturdier species as seed or pollen parents, through years of testing and elimination of the weaker, or less hardy, plants, many new hybrid strains will grow and perform well where one, or sometimes both, of the parents may be grown only with the greatest difficulty, if at all ... Like the mule that has more strength and endurance than either of its parents, many of the hybrid lilies show more stamina and persistence than that commonly found among their ancestors.

Given the fact that evolutionary biologists so often emphasize that hybrids are inviable -- as in fact many are -- it's ironic that the phenomenon of hybrid vigor is so widely recognized by breeders. It is an extremely common, even typical, phenomenon.

Bluegill Lepomis macrochirus (click to enlarge)

In certain sunfish crosses (genus Lepomis) the hybrids are more vigorous and aggressive than their parents. Manwell et al. (1963) showed that this positive heterosis was, at least in part, the result of an enhanced blood chemistry, combining factors from both parents. Thus, synergy, the emergence of a new, nonintermediate trait as the result of the combination of two or more traits not previously associated in a single organism, often gives rise to nonintermediate traits in hybrids, just as the combination of two gases (e.g., hydrogen and oxygen) can produce a liquid (water). In this connection it is important to consider that the expression of any hereditary trait in any organism is the result of a complex interaction of molecules at the genetic level. In hybrids such interactions are of a novel, untried nature and can have unexpected effects.

Moreover, if a hybrid derived from a cross between two parents is crossed again with a third type of parent, the compound hybrid so obtained can have traits that are not intermediate between those of the first two parents. As we saw in the previous section, both domestic and wild compound hybrids are common. There are many examples of hybrids having trait not found in either of their parents. For example, hybrids between Audubons Oriole (Icterus graduacauda) the Altamira Oriole (I. gularis), which occur along the eastern border of the U.S. and Mexico, have streaking on their upper backs even though both their parents lack this trait.

Darwin and Heterosis. Even as a young man, Darwin was aware that hybrids need not be intermediate. In his Voyages of the Adventure and Beagle (1839) he remarks that

the mule always appears to me a most surprising animal. That a hybrid should possess more reason, memory, obstinacy, social affection, and powers of muscular endurance, than either of its parents, seems to indicate that art has here out-mastered nature.

Moreover, his later writings clearly show he was familiar with the phenomenon of heterosis. For example, the following extended (it continues to the end of this page) passage in Variation of Animals and Plants under Domestication (Darwin, 1868: vol. II, 129-131) shows that he knew nonintermediate hybrids had been repeatedly reported by a wide variety of breeders and investigators. It also provides some interesting examples.

With respect to the benefit derived from crossing distinct varieties, plenty of evidence has been published. [Augustin] Sageret repeatedly speaks in strong terms of the vigour of melons raised by crossing different varieties, and adds that they are more easily fertilised than common melons, and produce numerous good seed. Here follows the evidence of an English gardener: "I have this summer met with better success in my cultivation of melons, in an unprotected state, from the seeds of hybrids (i.e., mongrels) obtained by cross impregnation, than with old varieties, The offspring of three different hybridisations (one more especially, of which the parents were the two most dissimilar varieties I could select) each yielded more ample and finer produce than any one of between twenty and thirty established varieties.

Eugène Chevreul (1786-1889)

Thomas Andrew Knight — President of the Royal Horticultural Society. One of the first plant breeders to intentionally exploit heterosis.

[Thomas] Andrew Knight believed that his seedlings from crossed varieties of the apple exhibited increased vigour and luxuriance; and M. Chevreul alludes to the extreme vigour of some of the crossed fruit-trees raised by Sageret.

By crossing reciprocally the tallest and shortest peas, Knight says, "I had in this experiment, a striking instance of the stimulative effects of crossing the breeds; for the smallest variety, whose height rarely exceeded two feet, was increased to six feet; whilst the height of the large and luxuriant kind was very little diminished. Mr. Laxton gave me seed-peas produced from crosses between four distinct kinds; and the plants thus raised were extraordinarily vigorous, being in each case from one to two or three feet taller than the parent-forms growing close along-side them.

[Arend Friedrich] Wiegmann made many crosses between several varieties of cabbage; and he speaks with astonishment of the vigour and height of the mongrels, which excited the amazement of all the gardeners who beheld them. Mr. Chaundy raised a great number of mongrels by planting together six distinct varieties of cabbage. These mongrels displayed an infinite diversity of character; "But the most remarkable circumstance was, that, while all the other cabbages and borecoles in the nursery were destroyed by a severe winter, these hybrids were little injured, and supplied the kitchen when there was no other cabbage to be had.

Mr. [Benjamin] Maund exhibited before the Royal Agricultural Society specimens of crossed wheat, together with their parent varieties; and the editor states that they were intermediate in character, "united with that greater vigour of growth, which it appears, in the vegetable as in the animal world, is the result of a first cross." Knight also crossed several varieties of wheat, and he says "that in the years 1795 and 1796, when almost the whole crop of corn in the island [i.e., Britain] was blighted, the varieties thus obtained, and these only, escaped in this neighbourhood, though sown in several different soils and situations.

Austrian Pine — Pinus nigra (click to enlarge)Credit: Andre Engels

Scot's Pine — Pinus sylvestris (click to enlarge)

Joseph Kölreuter — One of the first scientists to document heterosis in plants

Here is a remarkable case: M. Clotzsch crossed Pinus sylvestris [Scot's pine] and nigricans [now Pinus nigra, Austrian pine], Quercus robur and pedunculata [these two oaks are now usually treated as conspecific], Alnus glutinosa [European alder] and incana [gray alder], Ulmus campestris [English elm] and effusa [European white elm]; and the cross-fertilised seeds, as well as seeds of the pure parent-trees, were all sown at the same time and in the same place. The result was, that after an interval of eight years, the hybrids were one-third taller than the pure trees!

The facts above given refer to undoubted varieties, excepting the trees crossed by Clotzsch, which are ranked by various botanists as strongly-marked races, sub-species, or species. That true hybrids raised from entirely distinct species, though they lose in fertility, often gain in size and constitutional vigour, is certain. It would be superfluous to quote any facts; for all experimenters, Kölreuter, Gärtner, Herbert, Sageret, Lecoq, and Naudin, have been struck with the wonderful vigour, height, size, tenacity of life, precocity, and hardiness of their hybrid productions. Gärtner sums up his conviction on this head in the strongest terms. Kölreuter gives numerous precise measurements of the weight and height of his hybrids in comparison with measurements of both parent-forms; and speaks with astonishment of their 'statura portentosa,' [luxuriance] their 'ambitus vastissimus ae altitude valde conspicua' [extreme height and girth]. Some exceptions to the rule in the case of very sterile hybrids have, however, been noticed by Gärtner and Herbert; but the most striking exceptions are given by Max Wichura who found that hybrid willows were generally tender in constitution, dwarf, and short-lived.

Kölreuter explains the vast increase in the size of the roots, stems, etc., of his hybrids, as the result of a sort of compensation due to their sterility, in the same way as many emasculated animals are larger than the perfect males. This view seems at first sight extremely probable, and has been accepted by various authors; but Gärtner has well remarked that there is much difficulty in fully admitting it; for with many hybrids there is no parallelism between the degree of their sterility and their increased size and vigour. The most striking instances of luxuriant growth have been observed with hybrids which were not sterile in any extreme degree. In the genus Mirabilis, certain hybrids are unusually fertile, and their extra-ordinary luxuriance of growth, together with their enormous roots, have been transmitted to their progeny. The increased size of the hybrids produced between the fowl and pheasant, and between distinct species of pheasants, has been already noticed. The result in all cases is probably in part due to the saving of nutriment and vital force through the sexual organs not acting, or acting imperfectly, but more especially to the general law of good being derived from a cross. For it deserves especial attention that mongrel animals and plants, which are so far from being sterile that their fertility is often actually augmented, have, as previously shown, their size, hardiness, and constitutional vigour generally increased.

However, Darwin's extensive knowledge of the effects of hybridization, and of heterosis specifically, is not reflected in the Origin, where he used the incorrect claim that hybrids are always intermediate to discount the idea that new types of organisms can be derived from hybridization. For example, every edition of the Origin published during his lifetime contained the following statement:

by crossing we can get only forms in some degree intermediate between their parents.

In this way a false claim became an axiom of subsequent evolutionary thought.