On the Origins of New Forms of Life
(Continued from the previous page)
Gametes. Gametes are specialized cells functioning in sexual reproduction. Many hybrids can reproduce even without engaging in sex (by means of apomixis or vegetative reproduction). For example, many can produce progeny by budding. But for those hybrids that have no means of reproduction other than sex, infertility (if it is severe) can be an effective block to propagation. Hybrid individuals of reduced fertility produce fewer gametes than pure individuals, and those that they do produce are more frequently defective than those of a non-hybrid individual.
In sexual organisms a gamete produced by the male parent fuses with a gamete produced by the female parent to initiate formation of a new individual. This event is called fertilization. The male gametes produced by animals and some plants (e.g., club mosses, horsetails, ferns) are called spermatozoa (plural of spermatozoon), or simply sperm. Their female gametes are called ova (plural of ovum). Ova are often called eggs. Most plants produce male gametes called pollen grains.
Gametes are generally produced in abundance. For example, a single milliliter of chimpanzee semen contains about 2.5 billion spermatozoa. Therefore, a hybrid may be extremely sterile in comparison with its parents, but still produce huge numbers of viable gametes. Thus, if a chimpanzee produced a hybrid with some other animal and that hybrid had one thousandth the fertility of its chimpanzee parent, it would still produce 2.5 million gametes per milliliter of semen. Plants, too, produce gametes in mass quantities. About the same number of gametes are contained in a single teaspoon of pollen as in a milliliter of chimpanzee semen.
The sheer quantity in which gametes are produced explains why many hybrids are partially fertile even when their gamete production is severely disrupted -- a small part of a very large number can still be quite a large number. Only a single male gamete is required to fertilize an egg.
Reciprocal Crosses. A reciprocal cross is one occurring between the same two types of organisms, but with sexes reversed. For example, a jackass crossing with a mare produces the common mule. But the reciprocal cross, between stallion and jenny, yields a different animal, the hinny, seldom produced by breeders.
Reciprocal crosses are not always of equal fertility. When domestic fowl cocks (Gallus gallus) fertilize guinea fowl hens (Numida meleagris), egg fertility is about 70 percent, but when guinea fowl cocks inseminate domestic hens, the fertility rate is only 12 percent (McCarthy 2006; Petitjean 1969).
Some crosses are easily obtained even when the reciprocal cross is not. Chaudhuri and Mandal (1981) studied reciprocal crosses between the Stinging Catfish (Heteropneustes fossilis) and the Walking Catfish (Clarias batrachus). When stinging catfish milt was applied to walking catfish eggs, the fertilization rate was 90 percent. But when walking catfish supplied the male gametes for fertilization of stinging catfish eggs, no fertilization was observed.
The fertility of the hybrid offspring (as opposed to the fertility of the cross itself in producing hybrid offspring) can also depend on the direction of the cross. Darwin (1859: 258) found it remarkable
that hybrids raised from reciprocal crosses, though of course compounded of the very same two species, the one species having first been used as the father and then as the mother, generally differ in fertility in a small, and occasionally in a high degree.
For example, when Michaelis (1954) used pollen from Epilobium hirsutum (Hairy Willowherb) to fertilize E. luteum (Yellow Willowherb), the resulting F1 hybrids were vigorous and fertile. However, when the cross was reversed, the offspring were abnormal in development and had sterile flowers.
Wishart et al. (1988) investigated male gamete production in hybrids between mule deer (Odocoileus hemionus) and white-tailed deer (O. virginianus). They report that an F1 hybrid sired by an O. virginianus buck produced mature gametes (though they were less numerous than in either pure parent and showed many abnormalities), while an F1 individual from the reciprocal cross produced none. Hybridization between these deer has produced a hybrid population that extends across the United States from Texas to Canada. Similarly, Finn (1907: 22) says F1 hybrids produced by a wood pigeon (Columba palumbus ) hen and domestic pigeon (C. livia) cock are partially fertile, but those from the reciprocal cross are not.
Studying reciprocal crosses in the salamander genus Hynobius, Kawamura (1953: 112-114) found that H. nebulosus females produce hybrids that are partially fertile in both sexes when crossed with H. nigrescens, but noted that "a nearly complete gametic isolation seems to be present between nigrescens females and nebulosus males." In this cross, then, reversal of the sexes has a radical effect on the outcome of the cross. In one direction it produces partially fertile hybrids of both sexes, but in the other the male gametes cannot even fertilize the eggs.
"Nonreversible" reciprocal crosses of this sort constitute one of the many difficulties that arise when one concerns oneself with whether populations should be treated as conspecific (see Section 1.9). According to a biological definition of species, male and female individuals of H. nigrescens should be treated as conspecific. However, should nebulosus males be treated as conspecific with nigrescens females if the male gametes of the former cannot even penetrate the female gametes of the latter?
Variation in the Fertility of Hybrids. The writer's surveys of published reports of avian and mammalian hybridization (McCarthy 2006; McCarthy, in prep.) have revealed a general tendency on the part of researchers to make black-and-white assessments of hybrid fertility. If an investigator doesn't observe offspring from a hybrid of a particular type, they will likely conclude all hybrids of that type are sterile. If another observer looks at a hybrid of the same type and finds it does produce some offspring, they will likely express the opinion that all such hybrids are fertile.
However, the actual ability of hybrids to produce offspring varies from cross to cross, and, for a particular cross, from individual to individual. Within the context of stabilization theory, this fact is important since it opens up the possibility of natural selection among differing hybrids. Therefore, this phenomenon will be considered here at some length. Variation of this sort has long been recognized. After noting that fertility is usually lower in hybrids than in their parents, Stebbins (1969: 33) pointed out that
the majority of interspecific hybrids, however, are not completely sterile, but are able to produce at least a small percentage of viable gametes, at least of one sex. In the F2 or back cross progeny of such hybrids a great range of fertility exists, and in nearly all such progenies there exist some individuals which are more fertile than was the F1. This fact was already demonstrated many years ago by Müntzing (1930) in his research on Galeopsis tetrahit × bifida, and has been found in the progeny of many other F1 interspecific hybrids (Stebbins, 1950; Grant, 1963).
Stebbins' experience was primarily with plants, but the writer's own surveys of avian and mammalian hybrids has revealed the same variability in fertility, especially in later generations, in a wide variety of crosses. So this phenomenon appears to be characteristic of hybrids produced by a very broad range of organisms.
The fact that there is variation in fertility even among hybrids derived from the same original cross is important because, as Goldman et al. (2004) point out, there is a "common perception of the reduced fitness of hybrids." Certainly, on average, hybrids are less able to survive and reproduce. However, there is a range of fitnesses in hybrids. Those hybrids at the upper end of the range will be favored by natural selection. Fertility often increases with backcrossing. In captive crosses, this is one of the most frequently observed pathways to fertility.
Thus, hybrids, known as beefaloes (or cattaloes), can be produced from the cross domestic cattle (Bos taurus) × American Bison (Bison bison). Beefalo males, produced by the first backcross are usually sterile, but when partially fertile backcross females are backcrossed again, the resulting males are frequently fertile. Similarly, in the cross Chrysolophus pictus (Golden Pheasant) × Lophura nycthemerus (Silver Pheasant) the males are partially fertile, but the females are virtually always sterile. When the fertile male hybrids are backcrossed to L. nycthemerus, however, some of the females so produced are also partially fertile. In point of fact, in many crosses the hybrids are already partially fertile in both sexes even in the first (F1) generation.
Although most types of hybrids are less fertile than their parents, the degree of fertility varies widely according to the cross in question, from crosses producing very infertile hybrids, unknown to produce offspring, to crosses producing progeny about as fertile as either parent. Even hybrids between genera can be fertile. For example, some crosses between Aronia (chokeberries) and Sorbus (whitebeams, rowans, service trees, and Mountain Ash) produce hybrids that Christopher et al. (1991: 343) say are "completely fertile" while others result in infertile hybrids that produce fruits that contain few seeds. Darwin noted long ago that hybrids
are very generally infertile in some degree. But besides the extreme difficulty of deciding in some cases what forms to rank as species & what as varieties, we shall see that there is so insensible a gradation from utter sterility to perfect fertility that it is most difficult to draw any distinct line of demarcation between the two; -- more especially as other quite independent causes often simultaneously tend to give some degree of infertility. In some very few cases it is, I think impossible to withstand the evidence that forms which are universally admitted to be good species are quite fertile together & produce quite fertile offspring.
In fact, today it is known that many thousands of crosses between organisms treated as separate species produce hybrids that are themselves capable of producing offspring.
The degree of fertility varies, too, with gender, and, as we have already seen, with the direction of the cross. It can often be improved in successive generations by selection and backcrossing. Stebbins (1959: 237) points out that
the offspring of many partly sterile hybrids are more fertile than the F1, and this fertility often increases in later generations.
Given this variability, the failure of one, or even several, individuals to produce offspring does not guarantee another hybrid produced from the same cross will also be unsuccessful. In the cross between common sunflower (Helianthus annuus) and Jerusalem artichoke (H. tuberosus), Marchenko (1962: 321) produced a large number of backcrosses to both parental plants and examined approximately 10,000 seed heads from these hybrids. Among these, only a few with a single seed were found. However, one of the plants produced by backcrossing the F1 to H. annuus produced 700 seeds, thus providing Marchenko with starting material to breed rust resistance in the sunflower. Thousands of other plants from the same cross were either sterile or produced one or two seeds per plant.
As was just mentioned, the sex of a hybrid can also have a bearing on its fertility. For example, when two types of mammals cross and one sex is absent, rare, or of reduced fertility among the hybrids, it is virtually always the male. The reverse is true among birds. In other classes of organisms, however, no such bias occurs. Thus, F1 male beefaloes are virtually always sterile, but the females are partially fertile and can be backcrossed to domestic or bison bulls.
However, in those classes of organisms where such biases occur there is a continuum of cases. For example, in some avian crosses, females are as common as males and lay fertile eggs. In others, they lay sterile ones. In still others no females are produced at all. Bhatnagar (1968) reported that when common pheasants (Phasianus colchicus) were mated with domestic fowl (Gallus gallus), the male-female ratio in hatched eggs was about 12:1. In a study of quail-chicken hybrids (Coturnix japonica × G. gallus), Takashima and Mizuma (1982) found that 74 percent of the surviving hybrids were male after three days of incubation, and 90 percent, after five. After hatching, all were male.
Although fertility in hybrids is a matter of degree, reports for most crosses offer no exact quantification of this characteristic. Most crosses are poorly evaluated with regard to the viability of offspring. For example, in a review of avian hybridization Gray (1958) lists a single report for European Greenfinch (Carduelis chloris) × Yellowhammer (Emberiza citrinella). She describes results for a single clutch of five eggs. Three eggs were sterile, one hybrid died in the shell, and one survived to maturity. On the basis of such limited data, no firm conclusions could be reached concerning the general viability of offspring produced from this cross.
Even within a population treated as a single species, fertility varies from one individual to another. For example, individual human beings vary markedly in fertility. The same is true of individuals participating in hybrid crosses. Individuals sterile when mated with their own kind will likewise not produce progeny when participating in a hybrid cross.
To some extent, hybrids are subject to the same constraints as other organisms. For example, they can be too young, or too old, to breed. They can also refuse to breed because it is the wrong season or because of stress induced in captivity, or because their needs have not been met in some other way. How well a given cross works, then, depends in part on which individuals mate, as well as the conditions under which the mating is attempted. This fact has long been recognized. Darwin was well aware of it:
The fertility, both of first crosses and of hybrids, is more easily affected by unfavourable conditions, than is the fertility of pure species. But the degree of fertility is likewise innately variable; for it is not always the same when the same two species are crossed under the same circumstances, but depends in part upon the constitution of the individuals which happen to have been chosen for the experiment. So it is with hybrids, for their degree of fertility is often found to differ greatly in the several individuals raised from seed out of the same capsule and exposed to exactly the same conditions.
For example, Takahashi (1982) studied interfamilial hybrids (Numididae × Phasianidae) between guinea hens (Numida meleagris) and three different types of chicken cocks (White Leghorn, Nagoya, and Barred Plymouth Rock). He found that the number of fertile eggs was not the same from hen to hen. Instead, the hens showed a broad range of receptivity.
As Darwin notes in the passage just quoted, uniform fertility is no more the expectation in hybrids than in the crosses producing them. Many known crosses produce hybrids that are capable of producing offspring. But different hybrid individuals produced by a single type of cross can differ in fertility even in the F1 generation (which is generally much less variable than later hybrid generations).
The cross Sterlet (Acipenser ruthenus) × Beluga (Huso huso), two types of sturgeon, provides an example. Kijima et al. (1988) examined the testes and ovaries of hybrids of this kind and found significant variability. In some F1 individuals, the gonads were undifferentiated, but, in others, were fully developed and contained mature gametes. Certainly, some individuals produced by this cross are able to produce offspring; an earlier article reported F1 hybrids mated among themselves to produce an F2 generation.
Goodspeed (1915) found that most varieties of common tobacco (Nicotiana tabacum), when crossed with the weed N. glutinosa, produce hybrids of relatively low fertility, only about 10 viable seeds per capsule. But Clausen and Goodspeed (1925: 279) found that when a variety of N. tabacum from Cuba was crossed with N. glutinosa the hybrids produced seed "of the same order of viability as the pure seed of the species."
Therefore, when evaluating the fertility of a given cross, it is better to reserve judgment until a variety of individuals have been tested. Even then, a degree of uncertainty remains. As Darwin (1859: 256) points out,
There are species which can be crossed very rarely, or with extreme difficulty, but the hybrids, when at last produced, are very fertile.
A good example of the need for caution is the cross of barbary sheep and domestic goat. After repeated efforts to cross various types of sheep and goat, Steklenev (1972) thought it safe to write the following: "Summarizing the results of hybridization of members of the sheep and goat genera with the use of both domestic and wild forms, we can conclude the impossibility of obtaining hybrids in a single one of the tested combinations." Among the crosses discounted by Steklenev is that between barbary sheep (Ammotragus lervia) and domestic goat (Capra hircus), which various researchers attempted to cross without success. Hybrid embryos were reabsorbed, or the fetuses, stillborn. Yet other breeders eventually succeeded in delivering a healthy, partially fertile male hybrid. Moore et al. (1980) say its semen contained about 2 × 109 spermatozoa/ml, with excellent motility.
Often, the fact that a cross has not been reported merely reflects that no effort has been made to obtain it, or that the necessary technology has been lacking. Thus, with regard to lilies Rockwell et al. say that
For centuries no attempts were made to get the natural species, the wild lilies, to cross. This was not due to the fact that members of the lily tribe were incompatible. It was, rather that the natural species come into flower over a very wide period of time -- early June to late September -- thus reducing the range of possible artificial crosses. Now, with modern methods of preserving pollen by cool and dry storage, almost any two species may be crossed.
The ability to cross varies not only with the types that are crossed, but can even vary for the same individual at different times. Olsen (1972) notes that the frequency of fertile hybrid eggs decreased over a 15-week period as turkey hens developed antibodies to chicken spermatozoa. Similarly, McGovern (1973) reported an acceleration in deaths of goat (Capra hircus) × sheep (Ovis aries) hybrid ("geep") embryos, when the mother goats had earlier received skin grafts from sheep and injections of ram leukocytes. A female geep was produced by a serendipitous mating of a ram and a nanny goat (Cribiu et al. 1988; Tucker et al. 1989). It birthed a healthy backcross hybrid after mating with a ram. However, Tucker et al. say later attempts to breed the same geep were unsuccessful due to embryonic mortality, again suggesting antibodies had been produced. Depending on the cross, then, individual fertility may be a continuum grading from the most fertile hybrid in a population to the most sterile.
Sometimes hybrids are more crossable, and thus in a sense more fertile, than their parents. For example, Rockwell et al., who were just quoted in connection with the many recent reports of new lily hybrids, say that
This recent breakthrough in lily hybridizing, however, has also been due to the fact that, although the natural species showed marked resistance to being crossed, their hybrid offspring did not. They crossed readily not only with one another, but also back again with the natural species. In recent years, as a result, the floodgates to new lilies, and even to distinctly new types of lilies, have been opened. We now face the day when we shall have a plethora of new lilies." [italics appear in original]
Nevertheless, when it comes to fertility, the writer's experience indicates that many people perceive hybrids in a stereotypic manner. They think of the common mule as soon as hybrids are mentioned. Moreover, they go on to suppose that all mules are absolutely sterile and that this supposed absolute sterility of mules is characteristic of all hybrids. In this way, a mistaken idea concerning the characteristics of a single type of hybrid (i.e., the notion that all mules are absolutely sterile) expands to become a mistaken belief about a broad class of organisms (i.e., the belief that all hybrids are sterile).
As we have seen, many hybrids are partially fertile. Moreover, even the specific case of the mule is far from hopeless. While mules are typically of very low fertility in comparison with many hybrids, there have been numerous reports, some of them completely reliable, of mare mules producing offspring. Here in the United States, apparently, no one even tries to breed mules, but, according to Rong et al. (1985: 821), "in China, where mules are bred intensively by artificial insemination, there has been no doubt that the animals are occasionally fertile."
Variation in the Viability of Gametes. That hybrids produce abnormal gametes has long been known. Even Darwin was aware of the fact. Thus, he says that in hybrid plants
the pollen is manifestly imperfect as may be seen by everyone who has ever examined a hybrid. In like manner, with hybrid animals the spermatozoa are imperfect."
In a purebred individual one gamete typically looks much like the next. But in hybrids they often vary in size and shape, and many are inviable.
For example, although beefalo males do not usually produce viable gametes in the F1 generation, when partially fertile female hybrids are backcrossed, second and third generation male backcrosses do produce sperm, and are fertile in varying degree. Their gametes are abnormal, varying in shape and size even within the ejaculate of a single individual.
Close et al. (1996) describe many defects in the sperm of hybrid rock wallabies (Petrogale), which included such abnormalities as multinucleate, irregularly shaped, markedly enlarged, or multiple-tailed spermatozoa. The degree of variability present in hybrid spermatozoa can itself vary from one hybrid individual to another.
In studying the cross American bison (Bison bison) × domestic cattle (Bos taurus), Shumov and Rubtsov (1981) note that gametes from ejaculates of one hybrid (3/8 bison - 5/8 domestic) were virtually all normal in structure and motility, but that the ejaculates of another (a 3/4 bison - 1/4 domestic) bull contained very few gametes and virtually all were structurally abnormal.
According to Steklenev (1983: 62), an American Bison crossed with an F1 hybrid from the cross yak × mithan (Bos grunniens × Bos frontalis) produced a three-way hybrid that exhibited "a comparatively normal course of spermatogenesis" with a sperm density of 4.29 million/ml, but 35 percent of its gametes were abnormal.
In a plant hybrid of low fertility some of the pollen grains may be abnormally large, but most, though variable in size, will be much smaller than in a fertile plant and devoid of contents. hybrids often produce a high proportion of empty seeds. Stains are widely used to detect infertile pollen because they differentially color the empty grains. For example, the malachite green-acid fuchsin-orange G stain of Alexander (1969) stains fertile pollen red, and infertile pollen green.
A Fallacious Assumption. Given the facts thus far presented on the fertility of hybrids, it must be clear to the reader that many hybrids of unevaluated reproductive status would turn out to be partially fertile if they were tested. Additional evidence yet to be presented, will further tend to confirm this conclusion.
However, many people, when confronted with a hybrid, will assume it is sterile unless they are provided with evidence to the contrary. This presumption that hybrids of unknown reproductive ability are sterile, is one of the tacit presuppositions mentioned in the Introduction. It can have a potent effect on one's theoretical outlook. Since the great majority of hybrids have not been evaluated with respect to fertility, it leads one to presume most hybrids are sterile, an assumption that, in turn, prompts the conclusion that hybrids are, in general, evolutionary dead-ends. Likewise, anyone who believes that forms should not be treated as distinct species if they produce hybrids that are not perfectly sterile, will think that any two forms producing partially fertile hybrids should be treated as belonging to the same species.
This assumption that hybrids of uninvestigated reproductive status are sterile (combined with the additional widespread misconception that hybrids are rare in a natural setting) makes hybrids seem far less interesting than they otherwise might. In fact, I am sure such presuppositions have gone far in preventing the study of hybrids. After all, from such a perspective, hybrids are freakish, sterile aberrations that can tell us little about natural processes and the ordinary course of evolution.
This preconception can be self-perpetuating -- since many people think hybrids are irrelevant, they lack the interest to learn more and find out that such is not the case. The curiosity is also often lacking that might otherwise prompt researchers to conduct studies that would provide additional evidence that partially fertile hybrids do occur in the wild. NEXT PAGE >>
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