4.11: Recombinational Stabilization
(Continued from the previous page)
Recombinational Stabilization. In recombinational stabilization a variable, interbreeding hybrid population produces a new, stable type of organism without the addition of chromosome sets. As we have seen, many natural hybrid populations are composed of partially fertile individuals. In such sexual populations, due to the production of a broad spectrum of later-generation hybrids, genetic variation is quite high. Because such populations contain variable individuals capable of producing offspring, they are subject to natural selection just as are populations unaffected by hybridization. The only difference is that hybrid populations are far more variable. So most of the natural selection processes described in conventional population genetics also apply to hybrid populations, even though such processes are typically thought of as occurring in pure, reproductively isolated populations. Indeed, they are more applicable; for the rate of genetic change resulting from selection is proportional to the genetic variance of the population (Fundamental Theorem of Population Genetics). Hybrid populations almost always have higher genetic variances than pure parental populations, usually far higher. So the potential rate of evolutionary change in hybrid populations is extremely high. In particular, fertility is variable in hybrid populations.
In general, as has already been stated (see Section 2), sexually produced progeny of F1 hybrids are usually highly variable, whether they are produced by matings among the F1 hybrids themselves or from backcrosses to the parents. The same is true of the progeny of hybrids in subsequent generations. But breeders often report that hybrid stocks maintained for many generations become less variable over time. For example, Brilmayer (1960: 188) notes that the ricinifolia begonia (Begonia ricinifolia) which is derived from a hybrid cross (B. heracleifolia × B. peponifolia), yields fairly uniform progeny when self-fertilized because its "characteristics have become established over a long period of time."
Selection among the highly variable progeny descended from a hybrid cross allows breeders to combine traits previously found only separately in the two parents from which the hybrids were derived. As Rockwell et al. (1961) point out,
"Hybridization, the breeding of new lilies, then, is not an idle pastime of the curious gardener or of the grower who wants to cross two lilies and raise the seed to the flowering stage just to see what will happen. It is a deliberate attempt to raise hardier lilies, more able to endure adverse conditions, more adapted to the garden; flowers which should retain many of the virtues of both parents, but lack most of the bad qualities. The ideal solution, that of combining all of the good qualities and eliminating all the faults, shall probably never be attained. In many of the new lilies, however, so much improvement has been made that the value of hybrid lily strains, as compared to the true species, has been proved to the satisfaction of all experts and gardeners."
Recall that breeders use the word strain to distinguish hybrid derivatives that are sufficiently fertile to maintain themselves by sexual reproduction. Obviously, within such strains, individuals that are more fertile will tend to produce more progeny. Therefore, within such strains fertility will tend to improve over time since it is itself a heritable trait. The fact that fertility tends to improve under the influence of artificial selection without the production of polyploids in later-generation hybrids has long been known. This phenomenon has been repeatedly reported by a variety of authors. Even Darwin (1868: vol. II, 110) mentions what may have been a case
"given by M. Groenland, namely, that plants, known from their intermediate character and sterility to be hybrids between Ægilops and wheat, have perpetuated themselves under culture since 1857, with a rapid but varying increase of fertility in each generation. In the fourth generation the plants, still retaining their intermediate character, had become as fertile as common cultivated wheat." [italics are Darwin's]
Five pages later, he states, in connection with "the influence of free intercrossing" of plants and animals under domestication, that "if additional vigour and fertility be thus gained, the crossed offspring will multiply and prevail."
In Variation (1868: vol. II, 109) he says the idea that selective breeding under domestication eliminates sterility in domestic breeds derived from hybridization "was first propounded by Pallas," the eighteenth century naturalist. In the Origin Darwin expressed his belief that not only plant hybrids could recover their fertility under domestication, but also those of animals:
"The various races of each kind of domesticated animal are quite fertile when crossed together; yet in many cases they are descended from two or more wild species. From this fact we must conclude either that the aboriginal parent-species produced at first perfectly fertile hybrids, or that the hybrids subsequently reared under domestication became quite fertile. This latter alternative, which was first propounded by Pallas, seems the most probable, and can, indeed, hardly be doubted. … According to this view of the origin of many domestic animals, we must either give up the belief of the almost universal sterility of distinct species of animals when crossed; or we must look at sterility, not as an indelible characteristic, but as one capable of being removed by domestication."
Elsewhere he comments in a similar vein:
"But as with our domesticated animals, a cross-breed can certainly be fixed and made uniform by careful selection in the course of a few generations, we may infer that the free inter-crossing of a heterogeneous mixture [i.e., a hybrid population] during a long descent would supply the place of selection, and overcome any tendency to reversion; so that the crossed race would ultimately become homogeneous, though it might not partake in an equal degree of the characters of the two parent races."
Natural selection would be expected to act in a similar manner within the context of natural hybrid populations to favor the emergence of fit, fertile strains as new, reproductively stable somatypes. And various natural somatypes are in fact known to have had such an origin. Studies with plants (Gallez and Gottlieb 1982; Grant 1966a, 1966b; Rieseberg 1991; Rieseberg et al. 1990; Stebbins 1957; 1958: 183) have shown that such fertile derivatives can even be reproductively isolated when backcrossed to the parental types from which they are derived (backcross hybrids of low fertility are produced), a finding that has led some to refer to these derivatives as a "species."
Such ideas are anything but new. Long ago Lotsy (1916) pointed out that the complex variation resulting from wide crosses could potentially provide an extraordinarily rich genetic variability on which selection might act. Although it has not been widely accepted among evolutionists, the production of new forms by this method is commonplace among breeders. It should be said, though, that the notion has had a few major proponents over the years, even among evolutionists themselves. For example, in considering possible sources for the high degree of genetic variability required for rapid macroevolutionary change, Stebbins (1959: 248) asserted that:
"because of the slow rates at which it occurs, mutation can never provide by itself enough variability at any one time to fulfill such conditions. Genetic recombination must therefore, be the major source of such variability so that the evolutionary lines most likely to take advantage of a changing environment are those in which recombination is raised to a maximum. This is accomplished most effectively by mass hybridization between populations having different adaptive norms."
Similarly, Lewontin and Birch (1966) asserted that "the introduction of genes from another species can serve as the raw material for an adaptive evolutionary advance."
Nevertheless, this notion has never gained wide acceptance among biologists. In the writer's opinion, biologists have not rejected the idea because they are unaware that many hybrids can produce offspring or that hybrid populations are typically more variable than populations unaffected by hybridization. On the contrary, most seem to be conscious of these facts. Rather it seems they have failed to embrace Stebbin's view because it conflicts with a core tenet of neo-Darwinism: the consensus belief that forms treated as species typically arise as gradual change occurs in groups of interbreeding individuals reproductively isolated from other such groups. Recall that neo-Darwinian theory says macroevolutionary change occurs through selection of traits existing within each isolated population. To accept Stebbin's suggestion would be to reject neo-Darwinism's conception of macroevolution at a fundamental level because he is asserting evolution is more likely to occur rapidly in hybrid populations than in isolated ones. Therefore, when a biologist who accepts neo-Darwinian theory hears hybrids of a certain type produce offspring in a natural setting, she must assume those offspring lack potential. Not to do so would be to begin to think in a whole different way. Perceiving the world through neo-Darwinian glasses, she does not think in terms of how natural selection might affect the hybrid population over time. Instead, merely by assuming reproductive isolation of the parental populations is as yet imperfect, she dismisses the fact that hybridization is producing fertile individuals. She knows quite well that orthodox theory says evolution occurs within parental populations, not hybrid populations. So even though it is known that a broad array of hybrids are partially fertile and that a huge number of such populations occur in a natural setting, she pays little attention to these facts and goes on thinking as before. Neo-Darwinists assume any fertility seen in hybrids is residual and that it is in the process of elimination because, in their view, the parents have not yet become perfectly isolated. And, of course, there are many uninformed people who hold the stereotypic view of a hybrid as something absolutely sterile and not occurring in a natural setting. These, too, will easily dismiss Stebbin's assertion.
Nevertheless, it is now well known that a new type of organism can emerge, without the addition of chromosome sets (i.e., without the production of polyploids), as a stable population of interbreeding individuals within the context of a variable, interbreeding hybrid population. These new derivatives are selected artificially by the breeder for fitness and fertility; in the wild they are naturally selected. In a formal biological setting the process producing such stable derivatives goes under a variety of names: "recombinational speciation," "allohomoploid nothospeciation," or "stabilization of segregates." Here we will call such products recombinant derivatives, because they recombine portions of the genetic material found separately in their parents. The process that produces such derivatives that produces such derivatives is recombinational stabilization. Breeders seem to lump all types of fertile hybrid derivatives indiscriminately under the name strain, so they would use that name for a recombinant derivative. However, breeders, who are more interested in the fact of fertility, are often less exact in their choice of terms, than biologists who are interested in the underlying genetic mechanisms that produce the fertility. In particular, any fertile polyploid line would almost certainly also be called a strain. Breeders have produced innumerable recombinant derivatives (for practical purposes these recombinant strains can be distinguished from polyploid strains by the fact that their stabilization requires multiple generations, whereas polyploids stabilize almost immediately). Many natural recombinant derivatives have been treated as species. Indeed, among mammals and birds where cases of polyploidy and parthenogenesis induced by hybridization are virtually unknown, nearly all stabilized populations of hybrid origin must be of this type.
In general, any natural population will here be assumed to be a recombinant derivative when it (1) reproduces sexually; (2) is known to be of hybrid origin; and (3) is clearly not a polyploid. In subsequent discussion, two kinds of recombinant derivatives will be recognized: (1) those produced when distinct somasets of a single chromoset hybridize; and (2) those produced when distinct chromosets hybridize. In the case of such derivatives of intrachromoset matings, two somatypes cross to produce a variable population of hybrids. Under such circumstances, the hybrids are usually fully fertile even in the initial hybrid generations (since they are not structural heterozygotes). Once the hybrid population has been produced, individuals with certain genes can be artificially or naturally selected to stabilize a new somaset. In a natural setting, a degree of genetic isolation from the parental forms would be required for this process to lead to a new, uniform stable population. This partial isolation could be provided by any of the "prezygotic" mechanisms specified by standard evolutionary models — isolation by distance, behavior, ecological preferences, etc. Otherwise interbreeding with the parents would continue to influence the derivative hybrid population. For example, one could suppose two types of birds came into contact only on a particular island and formed a hybrid population there. Under such circumstances interbreeding might proceed to such an extent that eventually all individuals on the island would be hybrid. Natural selection could then proceed in the same way described in neo-Darwinism's account of evolution in a variable population. Even Darwin seems to have recognized that a degree of isolation assists the stabilization of new hybrid populations. In a letter to Fritz Muller dated January 1st, 1874, Darwin refers to "the fact of hybrids becoming more fertile when grown in number in nursery gardens." The footnote Darwin attached to this comment explains that "When many hybrids are grown together the pollination by near relatives is minimised."
Potentially any factor that prevented, or at least sufficiently reduced, matings between the hybrid and parental population would serve the same purpose. Meise (1936a) notes that in central and eastern Algeria there are huge, extremely variable populations derived from hybridization between the House and Spanish sparrows (Passer domesticus and P. hispaniolensis). However, he points out that in several isolated oases in southern Algeria and southwestern Tunisia only a stabilized derivative, flückigeri, of this hybridization is found. The isolation would not have to be of a geographic nature, such as in the example just given. It could also be based on behavioral tendencies or on habitat preferences—any factor that prevented ongoing backcrossing. Potentially, it could even result from the unlimited expansion of a hybrid zone until the pure parental individuals were entirely eliminated by interbreeding with hybrids—which would be the most extreme form of isolation conceivable. In such a case the remaining variable hybrid population could then undergo stabilization through selection. In the absence of such isolating factors, the hybrid population would continue to mate extensively with its parents and would continue to vary clinally, as in the typical hybrid zone, instead of becoming a uniform population.
A special case involves recombinant derivatives of interchromoset hybridization without the production of polyploids. Derivatives of this process have chromosome numbers having no simple relationship to the chromosome numbers of their parents, as is the case with polyploids. For example, Winge (1940) crossed two mustards, confertifolia and violacea-petiolata, usually treated as conspecific types under Erophila verna (spring draba). These types exhibit a large difference in chromosome number. The former has 15 chromosomes, while the latter has 32. Meiosis was disrupted in the F1 hybrids because many chromosomes were unpaired. As a result seed fertility was severely reduced (only about 3% of normal). The F2 generation was variable in morphology, fertility, and chromosome number. However, by the F9 generation, in some cases sooner, Winge was able to extract, reproductively stable, fertile, morphologically uniform recombinant derivatives each with one of six distinct chromosome numbers (n = 22, 23, 25, 29, 31, 34). Although, Winge did not carry out the experiments, if any of these derivatives were backcrossed to either parent, hybrids of reduced fertility would almost surely have resulted (due to reduced chromosome pairing).
Many biologists consider the stabilization of recombinant derivatives from interchromoset matings, to be of especial interest, because under such circumstances new forms of life can emerge that have all the characteristics usually expected of "species"—the emergent populations can have a new karyotype and be morphologically distinct, uniform, and be reproductively isolated. Referring to such derivatives, Stebbins (1958: 183) pointed out long ago that "the establishment [i.e., the production] of fertile, true-breeding lines from the progeny of partly sterile interspecific hybrids without change in the chromosome number [i.e., without the production of polyploids] has been accomplished in several genera of plants, and there is every reason to believe that it has occurred repeatedly as a natural phenomenon in plant evolution." Naturally occurring chromosets have since been genetically verified as recombinant derivatives of hybridization between other chromosets or even artificially re-created by crossing their parental chromotypes. Artificial recombinant derivatives produced in this way (perhaps not corresponding to any naturally occurring form of life) have also been extracted from interchromoset hybrids both by evolutionary biologists in a formal setting and by a wide variety of breeders. Moreover, computer simulations of natural hybridization between chromosets corroborate this inference and confirm the feasibility of stabilizing recombinant derivatives of interchromoset matings under natural conditions
When a recombinant derivative is produced from interchromoset matings, chromosomal mutations occur. The first chromosomal mutation that occurs during such a process is the combination of parental chromosomes in F1 hybrids. Because the parents are distinct chromotypes, their F1 hybrids are structural heterozygotes. As a result, meiosis in F1 individuals is disrupted and additional chromosomal mutations occur. Chromosomes are broken up and reconnected in new configurations as well as reassorted into new sets composed of chromosomes and genes previously present only in separate organisms. Such is the effect of structural heterozygosity on meiosis. Similar mutational events occur during meiosis in later-generation hybrids descended from such matings. Repeated crossing-over, breakage, repair, and reassortment (more chromosomal mutations) create restructured chromosomes and a reassorted karyotype in which genes from both parents are mingled (for example, see the analysis of Helianthus paradoxus carried out by Rieseberg et al. 1996). The newly combined genes in this new karyotype interact to specify the development of a new type of organism with a new combination of traits. The emergent chromoset can differ from its parental chromosets with respect to the structure of a single chromosome, or with respect to many. Recombinant derivatives produced from interchromoset matings do not require the assistance of prezygotic isolation factors to get established.
The Red Wolf (Canus rufus) of eastern North America is a recombinant derivative derived from hybridization between the coyote (C. latrans) and wolf (C. lupus). The cyprinid fish Gila seminuda (Virgin Chub) also had such an origin. It is derived from the cross G. elegans × G. robusta (Bonytail × Roundtail Chub). Pinus densata, a pine native to the Tibetan Plateau, is also a recombinant derivative, derived from hybridization between two other Asian pines: P. tabuliformis and P. yunnanensis. Another example is the perennial herb Penstemon clevelandii (Cleveland Penstemon), which occurs in southern California. It comes from hybridization between P. centranthifolius (Scarlet Bugler) and P. spectabilis (Showy Penstemon). The parents in this case differ markedly in their floral characters. P. centranthifolius has red trumpet-shaped flowers and P. spectabilis has broad tubular, bluish flowers).
Werth and Wagner (1990: 701) discuss Haberer's Groundpine, Lycopodium habereri, which is a recombinant derivative of the cross L. digitatum × L. tristachyum (Fan Clubmoss × Deeproot Clubmoss). This plant has spread over much of eastern North America. Wagner (1992) mentions two other clubmoss recombinant derivatives: (1) Lycopodium zeilleri (Zeiller's Groundpine), from the cross L. tristachyum × L. complanatum (Groundcedar); and (2) Lycopodium sabinifolium (Savinleaf Groundpine), from the cross L. tristachyum × L. sitchense (Sitka Clubmoss).
Two more examples are Argyranthemum lemsii and A. sundingii. These two shrubs have been described from the Anaga Peninsula, Tenerife, Canary Islands. Both are derived from hybridization between the same pair of parents, the coastal A. frutescens and the montane A. broussonetii. The parents differ markedly in morphology. This case is of interest because these two distinct stable recombinant derivatives treated as two separate species arose in separate valleys from the same parental combination (one parent being the pollen donor in the case of one derivative, but the other parent being the donor in the case of the other).
An example of a currently emerging animal recombinant derivative appears to be the hybrid population produced in New Zealand by interbreeding of the Mallard (Anas platyrhynchos) and the Pacific Black Duck (A. superciliosa). These hybrids are quite fertile and are increasing at the expense of their parents, which both seem headed for extinction in New Zealand. Hybrids are now more common there than is either pure parent. Gillespie (1985: 466) says that in the Otago region the proportion of pure black ducks "has declined from 100% prior to the introduction of the Mallard in 1867 to less than 5% in 1981." He also says the proportion of pure Mallards has been rapidly decreasing "in response to increasing hybrid levels." The hybrids are now in the majority in New Zealand and it seems likely they will soon swamp both their parents out of existence there and stabilize as a new type. Indeed, on the basis of specimens taken in the Marianas Islands, where hybridization of this kind also occurs, hybrids of this type have already been treated as a species, Oustalet's Duck (Anas ousteleti).
Such situations, where hybridization occurs in a geographically isolated region, probably assist the stabilization of new hybrid forms. Once the variable hybrid population fills the island environment to the exclusion of both parental types, selection within the population leads to the emergence of a new type just as in the models of genetically variable, reproductively isolated populations described in orthodox theory. There is little ongoing hybridization with the parents to maintain variation within the hybrid population. Isolation of such incipient forms can be ecological rather than geographic. Thus, Stebbins (1969: 30) says that "if the opening up of new habitats provides strong selective pressures in new directions, and if this condition is reinforced by any of a number of possible isolating mechanisms, the progeny of hybrids can respond to these new conditions by evolving in new directions more easily than can their parents."
Note however, that although recombinational stabilization occurs within the context of a hybrid zone, there is no reason to suppose that it must convert the entire hybrid zone into a new stable form. In general, a new stable type can emerge within the context of a hybrid zone even while the zone itself continues to exist (for example, polyploids often emerge within hybrid zones that continue to exist on an ongoing basis). Thus, recombinational derivatives can emerge as a cluster of individuals in one part of a hybrid zone and yet leave the remainder of zone unaffected (McCarthy et al. 1995).
On the other hand, many clinally varying wide hybrid zones have been treated as species or races. McCarthy (2006) lists many avian taxa of this kind. Grant (1981: 270) gives an example of a plant population of this type, the phlox Gilia achilleifolia (California gilia), which he says
"is believed to be of hybrid origin between some ancient members of the diploid G. capitata [bluehead gilia] and G. angelensis [chaparral gilia] groups … Gilia achilleifolia is intermediate morphologically between the putative parental species in every plant part. It is also extraordinarily variable in its morphological characters. This variability is expressed in the form of local racial differentiation. Some races of G. achilleifolia approach G. capitata in morphology, while other races approach G. angelensis. Indeed, the former races have been confused taxonomically with G. capitata and the latter with G. angelensis."
Though such populations have often been assigned scientific names, they do not have certain of the characteristics many biologists expect of a "species." For example, they are not morphologically uniform, and their members typically interbreed extensively with members of the parental populations. They may also lack stable karyotypic differences distinguishing them from other related groups. However, they do have some of the expected characteristics, so they are likely to be treated as distinct taxonomic entities: They are morphologically distinct from other types, have a separate geographic range (between the ranges of the parents), and such populations are stable in the sense that they continue to exist for long periods of time (i.e., they are temporally stable, although they are morphologically variable). Variable hybrid populations are temporally stable because the parental populations that interbreed to produce them are temporally stable. The stabilization process producing them is simply: (1) the initial contact of the parental populations; (2) subsequent interbreeding to produce a population of hybrids. Depending on the population in question, different degrees of stability and uniformity are reported. Presumably some of these populations, which are isolated by distance from their parents, have undergone selection. How often such populations will be treated as species depends on how stable, extensive, and distinctive they may be. It also depends, to a certain extent on the type of organism involved. For example, a botanist would probably be more likely to treat a known hybrid population as a species than would a zoologist.
New forms of life produced by the stabilization of hybrid populations are known from both captivity and the wild. For example, Restall (1997: 83) notes that although hybrids between the Bengalese (Lonchura domestica) and the Black Munia (L. stygia), two estrildine finches, were initially variable and of low fertility, they have been stabilized as various types that now breed true. Some of these recombinant derivatives have been officially accepted as new breeds of Bengalese. The South American butterfly Heliconius heurippa is a stable recombinant derivative of hybridization between H. melpomene and H. cydno. Mavárez et al. (2006: 870) say that two other butterflies, H. pachinus and H. timareta may also be derivatives of this cross. Gompert et al. found that the alpine butterflies in the Sierra Nevada of western North America (genus Lycaeides) were also hybrid recombinant derivatives. Pinoche Creek larkspur (Delphinium gypsophilum), which occurs in the valleys and foothills of California, is another recombinant derivative, from hybridization between foothill larkspur (D. hesperium) and Byron larkspur (D. recurvatum). ,
Recombinant derivatives produced from interchromoset hybridization have all the qualities usually expected of "species" because they represent chromotypes that are distinct from either of the parental chromotypes. Hybrids between the recombinant derivative chromotype and either of the two parental chromotypes are of reduced fertility because they are structurally heterozygous (see Section 3). Stebbins (1957) produced a stable recombinant derivative from interchromoset matings involving a strong sterility barrier. The cross was between Elymus glaucus (blue wildrye) and Elymus multisetus (big squirreltail). F1 hybrids between these grasses are highly sterile (less than 1% good pollen and only about 1 seed per 1,000 florets). The plants were backcrossed to E. glaucus and 173,000 florets from the resulting backcross hybrids produced 15 seeds, which yielded 11 mature plants. One of these eleven was partially fertile and had characteristics of both glaucus and multisetus. It was self-fertilized and yielded among its progeny vigorous, fully fertile individuals that yielded hybrids of low fertility when crossed with either of the original parents. In such cases a tremendous amount of human labor is required to extract a stable derivative. But the natural process requires no human effort. In a natural setting such plants are produced on a regular basis, year after year, generation after generation, wherever appropriate parental forms come into contact and produce hybrids.
Grant (1966a, 1966b, 1966c) also obtained such a derivative. The original cross was between the phloxes Gilia malior (scrub gilia) and G. modocensis (modoc gilia), which produce F1 hybrids with less than 2% pollen fertility due to structural differences between the parental karyotypes. Grant extracted stable, fertile recombinant derivatives from later-generation hybrids by selecting for fertility and vigor. The entire extraction process took about ten generations. All chromosomes were paired in the extracted forms, but some were derived from one of the original parents, and some from the other. As a result, hybrids from backcrosses of the derivative to either parent had karyotypes with some unpaired chromosomes. Therefore they were structurally heterozygous and quite infertile (see Chapter 3). For example, when one of the derivatives was backcrossed with G. malior, the resulting hybrids had 4 to 18 percent viable pollen and seed fertility of less than 1%. So the extracted form was reproductively isolated, to some degree, from both of its parents. This is why recombinant derivatives of interchromoset hybridization are more like what is usually thought of as a "species" than are derivatives of intrachromoset hybridization, where the derivative and the parents are usually completely interfertile. NEXT PAGE >>
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