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Animal Behaviour,
1991, 41:195-205
Wirt Atmar
(Received 4 December 1989; initial acceptance 12 March 1990;
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Abstract The observed mutation rate, m, is not the basal thermodynamic error rate affecting germline DNA but is rather the residual error that has passed uncorrected through cell-intrinsic error recovery mechanisms. Most of this nonrecurrent error will be purged from germline DNA through extrinsic selection, but at a measurable cost to the general competitiveness of the species. A primary reason for the existence of males in a bisexual species may be to act as a pre-zygotic filter of gene defects. Males appear to be an evolved auxiliary sexual caste that may be culled at less cost to the reproductive success of a species than by allowing both maternal and paternal lines of inheritance to be culled uniformly. A variety of genetical and behavioural mechanisms promote and exaggerate a general physiological fragility in male animals not apparent in females, haplodiploidy being the most obvious. However, explicit genetical mechanisms, such as haplodiploidy, which overtly expose error, may not be wholly necessary. The evolution of appropriately pugnacious combative behaviour in the diploid male may be sufficient. A single-locus gene in heterozygosis with a defect is immediately reduced to a 50% functional transcription rate. If such a defect can be exposed to selection, it will be made most apparent under metabolic stress. In vertebrates, metabolic exhaustion is a common theme in polygynous male-male intrasexual combat. Feeding is usually suspended prior to and during the period of contest, tending to increase overall metabolic stress further.
Introduction Protracted demonstrations of competitive vigour are common in male animals, especially in polygynous species. Any widespread behaviour must be presumed to have fundamental evolutionary purpose. The hypothesis to be argued here is: (1) rigorous demonstrations of vigour are a principal component of an extensive process that has been evolved to expose, exaggerate and expurgate significant gene error from the germline, and (2) that the evolution of the specific form of the vigour demonstration is intimately co-evolved with the physiological genetics of the enacting species. The observed mutation rate, m, is not the basal thermodynamic error rate affecting germline DNA, but is rather that residual error that has not been corrected by the error repair mechanisms of the cell. Most of this error will eventually be purged from germline DNA by extrinsic selection, although at a measurable cost to the general competitiveness of the species. Such a loss in fitness can be minimized by the evolution of a sexual caste that is ancillary to the primary line of descent. A principal reason for the existence of dimorphic/diethic males in a bisexual species may be to act as a pre-zygotic filter of genetic defects. A variety of genetical mechanisms promote a general physiological fragility in male animals not apparent in females, haplodiploidy being the most obvious. The value of males to a sexual species is otherwise unclear. Two distinct sexual castes are unnecessary to realize the advantages commonly ascribed to sexual recombination. A broad array of current hypotheses for the evolution and persistence of sexuality appears in Michod & Levin (1988). Yet for all of the variously postulated arguments, males are unneccessary. A single, monomorphic sexual caste of obligately outbred hermaphrodites could suffice. The paucity of such species in nature is prima facie evidence that males have assumed a role of greater evolutionary importance than that of simple mechanical complement to the female. Evolutionary optimization is a physical informational process. Error in transcription, replication and translation is inevitable. While evolutionary optimization is a greatly more complex and polygenic process than generally portrayed, defect infusion into the germline is a relatively simple process and reasonably well understood (Appendix I). Genetic defects are often expressed as pronounced phenotypic debilitations in certain individuals. The rate of potential error infusion into a germline is not trivial. Although the rate of uncorrected error per locus is relatively small (generally in the range of 0.00001 to 0.000001 errors per locus per generation), when this rate is multiplied by the number of actively translated loci and the ploidy number, the probability of that an individual will bear at least one novel mutation ranges from 0.005 to virtual certainty. If the functional collapse of the information held within the species' genome is to be prevented, mechanisms must be evolved to expurgate as much of this error from germline DNA as possible. The argument to follow is an extension of the Kodric-Brown & Brown (1987) hypothesis that much of that (Mendelian) point coding error can be expurgated from the germline pre-zygotically through the evolution of an auxiliary sexual caste in which that error has been exaggerated.
The Alternatives Point mutations are incorporated into a haploid genome at a rate greater than m per generation per locus. Some error can be detected and corrected without translation of the encoded message. Repair mechanisms are known to be active during gene replication, transcription, translation and subsequent protein manufacture (Hanawalt et al. 1978; Hanawalt et al. 1979; Gottesman 1981; Hall & Mount 1981; Little & Mount 1982; Cathcart et al. 1984; Lewin 1987; Friedberg & Hanawalt 1989). However, no finite set of information recovery mechanisms can detect, repair and recover all forms of error. For an error-repair mechanism to evolve, the form of the error must be frequent and recognizable. Genomic error occurs in two broad categories: optimization error and replication error. If the deme's statistically expected phenotype (the epiphenotype) is inappropriate to local circumstance (optimization error), the epiphenotype is reoptimized through selection to stochastically minimize overall phenotypic behavioural error. Replicative error (thermodynamically inevitable error in gene replication and expression), on the other hand, persists regardless of the quality of optimization achieved. If we assume that populations are optimized rather quickly, then it is replicative error that is of greater long-term competitive importance. Some error will pass through the most elaborate error repair procedures uncorrected. The same evolutionary pressures which promote the evolution of cell-intrinsic error correction protocols must be presumed to smililarly operate at higher levels of organization. The simplest high-order information assurance protocols are redundancy and stringent testing. Informational redundancy (polyploidy) increases the probability of proper genotypic expression within a single individual by mitigating the effects of an uncorrected point coding error. The expression of an alternate, functional allele is often sufficient to maintain viability, if not full competitiveness, of the individual. But polyploidy also simultaneously increases the likelihood of incorporating significant gene error into the germline. If the dose compensation of a polyploid defect is complete (complete recession), packets of non-functional or marginal code will be readily infused into the germline, subject to culling selection only when expressed homozygotically. Uncorrected polyploid gene error will pass generation to generation, hidden from selection. If we were to argue that informational redundancy is a potent technique to suppress gene error, then we should expect high-n autopolyploidy to be a commonly observed phenomenon, but it is not. Autopolyploidy is relatively infrequently observed in wild plants and is virtually unknown in animals (Appendix II). The Apparent Necessity of Hemizygosis The physical antithesis of informational redundancy is the stringent demonstration of phenotypic vigour. Vigour testing obtains maximal value only when the code set under consideration is absent of redundancy. All known eukaryotes engage some form of nuclear ploidy cycling, normally alternating diploid and haploid stages. Diploidy is a chromosomal redundancy state which apparently rests robustly between counterbalancing forces. Diploidy is the lowest ploidy state which will allow sexually-mediated chromosomal recombination; diploidy is simultaneously the highest ploidy state that can be reduced to haploidy in one meiotic step. In the haploid state, "uncovered" hemizygotic alleles, if translated, expose latent gene defects to selection. Male gametes are produced in far greater numbers than their corresponding female gametes. Sperm/egg ratios in the higher primates average about 100 million:1 per copulation (Smith 1984 and references therein). In both Metazoa and Metaphyta, sperm and pollen are smaller, more motile, more energy-restricted and placed more immediately at risk than the egg. Only one male gamete is paired with one ovum. All other sperm are functionally dispensible. At a minimum, nk distinctly chromosomally complemented haploid gametes may be created during gametogenesis, where n = ploidy number, k = number of chromosomes. A subvital allele, when reduced from a diploid state, will be present in one half of the gametes, potentially situated in 2k-1 genomes. The human vagina/cervix is an environment generally considered hostile to sperm (Smith 1984; Tortora & Anagnostakos 1984). Approximately 2000 human spermatozoa reach the site of the ovum, implying en route sperm extinction frequencies greater than 0.99999. If errors are to be selectively culled, the gametic phase is the least expensive point to perform that segregation (Stearns 1987). Sperm appear to be functionally required to run migration paths of evolutionarily enhanced stringency as a defect filter (Cohen 1973; Porter & Finn 1977; Appendix III). Rigorous intrapopulational sperm competition significantly decreases the probability that the single fertilizing spermatozoon will be metabolically impaired, abnormally chromosomally complemented, or otherwise incompetent. But what portion of the genome is open to defect exposure in haploid sperm? At present, the question cannot be answered precisely, although estimates can be made by indirect measurement. Gene function is described as either housekeeping or luxury. Luxury functions are those that are needed for specialized behaviour in the particular cell phenotype. In contrast, housekeeping functions are basally metabolic and are common to all nucleated cells. In the somatic tissues of higher-order eukaryotes the number of gene functions that are expressed is usually in the range of 10,000-20,000 and is probably never higher than 40,000. mRNA saturation experiments indicate an overlap of 50-75% (10,000-13,000 genes) between diverse tissue types in mammals and birds (Lewin 1987, chapter 17). If defects in these housekeeping genes can be exposed through a sperm vigour test, then substantial informational advantage can be achieved. An error in this basal genetic set would potentially impair the metabolism of every cell of the adult animal, immediately rendering the phenotype non-competitive. The ubiquity of such fundamental code exaggerates its critical nature. However, it is the evolution of adult haploid males that further extends and exaggerates the opportunity to expose significant gene error in the complete genome. Arrhenotokous haplodiploidy (Appendix IV) is a recurrent genetical invention, having evolved in Hymenoptera, many Thysanoptera, many mites, some Homoptera, several Coleoptera and at least one Rotifer. A haploid adult male demonstrates his lack of significant gene error as a vigourous hemizygote in ecological context. Alleles in a haplodiploid mating system are exposed to selection on the basis of the gender caste through which they pass. A physiological lethal present in the ovum of a diploid female is not informationally equivalent to a spermatozoic lethal derived from a hemizygotic male. Indeed, the spermatozoic lethal cannot exist by definition as it would also be lethal in the haploid male. Mating behaviour patterns do not need to be complex in haplodiploid species to screen gene error efficiently, they merely need to be rigorous. Aculeate Hymenoptera (bees, ants, wasps) exhibit characteristically strenuous mating flights. The female sets a rigorous flight course, and is followed by her haploid suitors. It would seem that she does not discriminate between males in any other way (Starr 1984). Metabolic exhaustion will expose even mild defects in a hemizygotic male which might otherwise pass unnoticed in a diploid heterozygotic female. The mating flight of aculeates has been argued for some time to be an effective filter of defects (Snell 1932, Kerr 1967, Eickwort 1969, Wilson 1971 p. 325, Starr 1984). The rate of gene defect purgation under panmictic haplodiploidy may be calculated. Let qt be the frequency of a measurable defect at time t, pt be the frequency of all other appropriate alleles, and s the selection coefficient against the defect. The defect frequency at time t+1 will be
The elimination of a lethal from a haplodiploid population is plotted in Fig. 1. Of significance, haplodiploidy does not intrinsically reduce the heterozygosity of neutral or heterotic alleles, as does diploid selfing or sibling mating, although all three patterns lead to a significant reduction of errors within the deme (Fig. 1).
Figure 1. Theoretical expurgation trajectories of a lethal allele (s = 1) calculated for various genetic patterns of inheritance. Initial heterozygosity (H = 1) for all calculations. A fully recessive lethal is most slowly purged from a panmictic population. As the recessive defect becomes rarer, it becomes increasingly "protected" by its rarity and the physiological sufficiency of a functional alternate allele.
Nuclear Ploidy Cycling The evolutionary advantage of cyclic reductions to haploidy cannot be ascribed to be either a necessary or consequential feature of recombination. Obligate outbreeding is not characteristic of extant primitive eukaryotes. Rather autogamy and automixis are common throughout lower-order eukaryotes (Raikov 1969; Allen & Gibson 1973; McDonald 1973; Sleigh 1973; Mogie 1986; Dick 1987) remaining common in phyla as complex as Bryozoa (Woollacott & Zimmer 1977) and some flowering plants. The most obvious result of nuclear ploidy cycling, generation to generation, is an informationally new infant zygote, apparently free of much potentially accrued somatic error. In ciliated Protozoa, ploidy cycles are relatively complex but may be informationally elegant. Germline DNA is sequestered in diploid micronuclei. Highly polyploid (16n to 13000n) (Raikov 1969) working DNA is replicated from the micronuclear genome at the beginning of each cell cycle into new macronuclei (Allen & Gibson 1973; McDonald 1973). All further cytosolic product manufacture is derived from macronuclear transcription (Sleigh 1973); the diploid micronuclei then become inert, apparently acting much like a "coding vault" for the inheritable genome. At the end of the cell cycle, the polyploid macronuclei are digested. Repetitive transcription, which entails repeated structural changes (melting) of the macronuclear DNA, is almost certainly mutagenic. Such DNA is likely to become corrupted and thus unreliable for purposes of inheritance. Prior to macronuclear digestion, the previously quiescent micronucleus is reactivated and undergoes both meiotic reduction and mitotic duplication resulting in two, four or eight haploid micronuclei. Only one micronucleus survives to become a gametic nucleus; all others disintegrate. If the survival of the one micronucleus is non-random but results from some form of coenocytic internuclear competition, the informational result is similar in effect to other demonstrations of functional haploid vigour. Aging in somatic cells has been generally thought to be analogous to the accumulation of error in germline DNA (Szilard 1959a,b; Sinex 1977; Sohal et al. 1985; but see Strehler 1977 Chapter 9). Higher-order eukaryotic tissue cell lines replicate only 40-70 times, irrespective of chronological age before decaying into functional senescence (Hayflick & Moorhead 1961; Orgel 1963; Hayflick 1965, 1966, 1977). Because repair mechanisms cannot correct all error, the senescence of a replicative cell line due to accumulated error is inevitable in the absence of stringent selection. Much of that culling selection will be extrinsic to the species (natural selection, however, some portion is clearly intrinsic to the species. The loss of competitiveness loss to the frequent manufacture of defective phenotypes can be minimized by the evolution of exaggerated pre-zygotic protocols of defect exposure and increased mating wariness in individuals (sexual selection, as defined by Darwin 1871, 1874, but not Fisher 1930; Appendix V).
Maximum Defect Expurgation Velocity is Defect purgation rates will reach extraordinary velocities when haplodiploid mothers mate with their demonstrably vigourous haploid sons. This mating pattern of haplodiploid selfing has been recently observed in the spider mite, Schizotetranychus celarius (Saito & Takahashi 1982; Saito 1987). Only S. celarius females overwinter, founding isolated populations in the spring. The unmated foundress oviposits a few haploid male eggs and then enters a period of quiesence, apparently waiting for her sons to mature. Little opportunity is presented for the sons to disperse, thus mating with the foundress is relatively certain. Her second brood of son-fertilized ova become diploid daughters. The probability of the passage of lethal or subvital recessive alleles by the foundress into the daughter population is reduced by the exposure of defective alleles in the haploid son/father generation, the males having acted as an auxiliary defect sieve. The rate of defect reduction, if the mother/son mating pattern were repeated indefinitely, is plotted in Fig. 1.
The frequency q of a defective allele, a, in a "selfing" haplodiploid maternal line of descent at time t+1 can be calculated. Let Pt , Qt , Rt represent the proportion of maternal diploid genotypes AA, Aa, aa respectively, where A represents all other fit alleles. At time t+1, the genotypes will occur in the following ratios:
Inbred haplodiploidy is not a condition apparently evolved by forced circumstance. The non-parasitic, strong-flying wasp, Eurodynerus foraminatus, which is readily capable of panmictic mating behaviour, has been observed to exhibit sibling mating frequencies of about 40% (Cowan 1979). Males eclose first and aggressively compete at the natal nest site. The victorious male drives off all of his brothers. He then inseminates each of his sisters as they emerge some days later. Inbred haplodiploidy implies genomes of exceptional purity and very rapid local race formation. Closed laboratory populations of haplodiploids often show no loss of vigour or competitiveness (Hoy 1977, 1985). Where inbred haplodiploid populations (both natural and laboratory) have exhibited difficulty, a depression in male frequencies (occasionally total) has been a common observation (Poe & Enns 1970; Alstad & Edmunds 1983).
Haploid males are extremely physiologically fragile by virtue of genetic construction, but much evidence exists that most diploid males are similarly more physiologically fragile than conspecific females, especially so in polygynous species where males are the heterogametic sex. Males in most metazoan species succumb more readily than females to disease, trauma, exhaustion and starvation (Widdowson 1976; Dauer et al. 1968; Klein 1968; Clutton-Brock 1985; Teather & Weatherhead 1989); suffer higher embryonic mortality rates (Poulson & Sakaguchi 1961; McMillen 1979; Hackett et al. 1986; Werren et al. 1986); die in greater numbers from accident and intrasexual combat (Iskrant & Joliet 1968; Clutton-Brock 1982; Daly & Wilson 1983; Jewell 1986); bear generally higher parasitic worm loads (Martin 1972; Schad & Anderson 1985); live shorter lives or are driven from the population after breeding, occasionally dying synchronously (Frisch 1954; Woolley 1966; Kerr 1967; Wood 1970; Braithwaite & Lee 1979; Eisenberg 1981; Barbault 1986). Polygynous males rarely care for their young, thus they become especially dispensible to the population in times of ecological stress and may be actively discriminated against during such periods (Montagner 1964; McClure 1981). Explicit genetical mechanisms, such as haplodiploidy, which overtly expose error in males, while efficient, may not be wholly necessary; the evolution of combative behaviour in the diploid male may be sufficient. The regulation of gene product titer is only casually limited by mRNA rates of transcription at metabolic rest. Where highly repetitive DNA exists, it is believed to have evolved to increase gene product synthesis during high transient demand (Brown 1981; Stark & Wahl 1984; Lewin 1987). Product deficiencies do not tend to become evident until more than 50% of the repetitive DNA has become non-functional. A single-locus gene in heterozygosis with a defect is immediately reduced to 50% functional transcription rate. If such a defect can be exposed, it will be made most apparent under metabolic stress. Human sickle cell trait appears to behave in this manner. The heterozygous condition has been generally considered a clinically benign state. However, human HbA/HbS heterozygotes appear to be at a 30-40x greater risk of sudden, unexplained death resulting from strenuous exertion, dehydration and hypoxia than a comparable population of normal homozygotes (Kark et al. 1987; but see Weisman et al. 1988). In vertebrates, metabolic exhaustion is a common theme in polygynous-male sexual behaviour. The contest is generally evolved to be as rigorous a demonstration of vigour as possible. Feeding is usually suspended prior to and during the period of male-male intrasexual contest, tending to further increase overall metabolic stress. Male excess mortality in some mammals appears to be directly and programmatically derived from androgenic hormonal levels, especially testosterone. Castrated human males live on average 13.6 years longer than unmodified men (Short 1985). Similarly, in feral Soay sheep (Ovis sp.), wether lambs (castrated males) significantly outlive both ewe and ram lambs. In contrast, mortality in normal males due to masculine behaviours is quite high. Although the sex ratio at birth is 1:1, adult ewes outnumber normal rams 5:1. The loss of gonads not only markedly alters the aggressive nature of the males but also diminishes behaviours that would otherwise promote high levels of physiological and nutritional stress (Jewell 1986). The complete recession of an allele is rare; heterozygotic loci normally express a phenotype intermediate to both homozygotes. Let t be the transparency of a defect in heterozygosis to selection, such that 0 £ t £ s. If t = 0, the defect cannot be detected as a heterozygote and the defect purge rate will be identical to panmictic diploidy. If t = s in metabolically stressed males and t = 0 in sessile females, the equation for defect purge rate is almost identical to haplodiploidy:
Purge rates are plotted in Fig. 1 for t = 0, t = 0.5s and t = s, when s = 1. The defect exposure coefficient t is not a selection coefficient necessarily imposed by extrinic circumstance, but is a value that is directly amenable to modulation by the species through the evolution of appropriately contentious and pugnacious behaviour in diploid males. As the operational sex ratio of a polygynous species is increased, a population of dispensible males is simultaneously enlarged. Males unable to hold territory, master a harem or otherwise sustainedly demonstrate vigour often exist on the periphery of the deme, suffering higher rates of mortality than mated males (Schaller 1963; Brown 1964; Kummer 1968; Estes 1969; Douglas-Hamilton 1973; Clutton-Brock 1982). Because most males in an optimized population will be genetically acceptable breeders, a surfeit population of floating, aggressive males insures that the few successfully breeding male(s) will not likely be significant gene defect bearers. To purge congenital error effectively from the deme, the polygynous species must evolve symmetric behaviour in the female such that she is sexually faithful to the subpopulation of proven males. This may happen indirectly, by the female selecting the quality of defended territory, breeding position or other species-idealized attribute rather than by focussing on simply the male(s) themselves (Searcy & Yasukawa 1982; Alatalo et al. 1984, 1986). Diploid Heterogamy is a Mild Form of Haplodiploidy In mammals, the male is the heterogametic (XY) sex while in birds, females are heterogametic (WZ). It may be no coincidence that polygyny predominates over monogamy in mammals, while birds exhibit a spectrum of mating types, ranging from polygyny to monogamy, and very rarely, polyandry. In both groups, one sex is haploid for two chromosomes (consisting of generally 2-8% of the bulk genotype) while the other gender is fully diploid. In human males, specific defects (colour blindness, hemophilia) are the result of known point coding errors on either of the X or Y hemizygotic chromosomes (McKusick 1975). Many other human genetic disorders are similarly sex-correlated. Some neurological defects (stuttering and autism) occur preponderantly in human males, the apparent result of impaired physiological development when absent of critical but unknown protein products. Errors are exposed more frequently in the heterogametic than the homogametic sex. Indeed, diploid heterogamy is a mild form of haplodiploidy. While the relative value of the anisogametic egg over the sperm weighs heavily in favor of the egg, the operational sex ratio very occasionally reverses in vertebrates and becomes polyandry. All true polyandrous species appear to be female-heterogametic. When the operational sex ratio does flip and becomes polyandry, a larger population of dispensible females simultaneously emerges. The present argument makes the strong prediction that heterogametic polyandrous females must assume the informational role of the polygynous male, thus becoming more transparently error-expositive (e.g. more brightly coloured, allowing pelage or feathering to become a measure of overall health or vigour), more physiologically fragile (more susceptible to disease and trauma), more aggressively combative and placed at greater risk. Tentative evidence for polyandrous birds (e.g. Höhn 1969; Jenni & Collier 1972) is consistent with this argument, evidence which Darwin (1874 p. 225) presumed to be true: "A few exceptional cases occur...in which the females instead of the males have acquired well pronounced secondary sexual characters, such as brighter colours, greater size, strength, or pugnacity. With birds there has sometimes been a complete transposition of the ordinary characters proper to each sex; the females having become the more eager in courtship, the males remaining comparatively passive... Certain hen birds have thus been rendered more highly coloured or otherwise ornamented, as well as more powerful and pugnacious than the cocks; these characters being transmitted to the female offspring alone."
I: The Nature of Mendelian Defects Metazoan genomes contain 5,000 to 50,000 actively translated genes. On average, 10-50% of the active genome appears to be translated in any one cell type. Constituent code representing basal cellular metabolism appears to be 50-75% of the code translated within all cells (10,000-20,000 gene functions in Deuterostomes, Lewin 1987 pp. 367-383). Much of this basal constituent code is presumed to be not characteristic of the species, but of the phylum, or higher, indicative of the antiquity of its origin. Tissue-specific code (another 10,000 to 20,000 gene functions in mammals and birds) is evolved hierarchically on top of this common platform. Any complex, well-conserved (h2 ® 0) structure (an eye, a heart, a stereotypical behaviour) results from the expression, directly or indirectly, of perhaps as much as 90% of the encoded genome. Gene effects do exist however which exhibit classical Mendelian ratios in phenotypes. Gross mendelian effects are virtually always defects. Complex physiologies can be brought to a halt through a single well-placed point coding error. An error, by its nature, is informationally trivial and isolated from the whole of the genome, and is thus segregatable through selection in a manner that no complex trait can be. Dwarfism is a common trait in domesticated plants and animals. In plants, dwarfism results from the unexpected absence of giberellic acids (GAs) (Goodwin & Mercer 1986 pp. 580-595). Although the trait often occurs in single-gene classical ratios, no "gene" for dwarfism exists. Nor do genes specifically exist for GAs. GAs are small-molecule metabolites, phytohormones, products of multi-enzyme circuits. A homozygously-expressed recessive defect within a single enzyme anywhere in the GA biosynthetic pathway may completely disrupt GA production. Dwarfism, like most defects, is a syndrome. Although the causal defect may always be traced a specific point coding error, an innumerable number of similar point errors will create approximately the same physiological deficiency. II: Gene Redundancy Multigene families are a common form of redundant coding which does not involve chromosomal polyploidy. A single gene is tandemly repeated many times (2-1,000,000 times). Multigene families are common for the abundant proteins; they appear to be maintained for production of critical product under high transient demand, although redundant coding simultaneously decreases the probability of the production of defective product. Much of the repeated code eventually becomes pseudogenetic (i.e. non-translatable due to one or more read-frame errors) or becomes reoptimized for other purposes. The sudden-correction and crossover-fixation models suggest that every so often a gene cluster is replaced by a new set of copies, derived from one or a very few copies present in the previous generation (Lewin 1987 pp. 420-421). III: Sperm Extinction Frequencies Sperm extinction frequencies from point of intromission to egg are unlikely to be the result of simple vigour segregation. Hunter (1987 1989; Hunter et al. 1983) provides indirect evidence that mammalian sperm capacitation and progression through the female genital tract is programmed by the endocrine activity of the Graffian follicle(s), sequencing the physiology of the female genital tract and the final maturation of the sperm as (1) a mechanism of sperm storage and (2) as a block to polyspermic penetration of the egg. The necessity of competency in the sperm to migrate through the tract is not called into question, but sperm numbers in mammalian oviducts at or shortly after ovulation appear to be actively regulated. Similarly, sperm agglutination near ripe eggs has been postulated for some time to be a mechanism to reduce the number of spermatazoa near the ovum(a), further minimizing the potential for polyspermy (Runnström 1952). IV: Haplodiploidy In arrhenotokous haplodiploidy, unfertilized ova become haploid males; fertilized ova become diploid females. The reciprocal condition, thelytokous haplodiploidy, is theoretically unstable and is unknown in nature. An informationally similar condition to arrhenotokous haplodiploidy known as parahaploidy exists in some phytoseiid mites (Helle et al. 1978). Both male and female embryoes are fully diploid, but males shed their paternal genome sometime prior to adulthood. The value of parahaploidy in exposing maternal germline defects to selection is identical to haplodiploidy. In all known cases where one or the other parental genome is eliminated, it is always the paternal genome. A somewhat related condition is physiological polyspermy, frequent in many animal groups (e.g. molluscs, reptiles and birds). Although several spermatazoa may enter the egg, only one participates in the development of the embryo. The egg possesses some mechanism to recognize and eliminate excess paternal nuclei. Similar but more exaggerated conditions exist in fresh-water unisexual fishes (Schultz 1969; Bulger & Schultz 1979). Hybridogenesis is a condition found in some all-female unisexual fish such that the paternal genome is non-randomly segregated and lost during meiosis. A new paternal genome is reintroduced at every generation through hybridization with a closely related congeneric species, only to be lost again at the next generational gametogenesis. Gynogenesis is a closely related form of "sexual parasitization" where congeneric sperm are necessary to induce cleavage of the unisexual's egg but the paternal genome is not incorporated into the zygote. No similar condition of genomic exclusion has ever been found to occur in mammals. The presence of the paternal genome appears to be essential to proper embryogenesis (Dawley 1989 and refs. therein). The evolution of haplodiploidy in mammals, although potentially beneficial, is thus prohibited. Haplodiploidy may similarly be prohibited in all vertebrates for other reasons (e.g. miscompensated gene dosages in a haploid phenotype), but a genetical system of inheritance combining aspects of both hybridogenesis and gynogenesis would potentially allow its evolution. Where haplodiploidy has evolved, it cannot be considered to be a rigidly stable genetic device; should for some reason the selective advantages of haplodiploidy be diminished, haploid males would almost certainly immediately disappear. In the honeybee (Apis mellifera), 8% of the emergent males are diploid (Woyke 1963, 1965a,b,c, 1967; Kerr 1969), fully complemented with both paternal and maternal chromosomes (Woyke & Adamska 1972; Michener 1974 pp. 71-73). The mechanism of expunging these diploid males from the population is not physiological but behavioural. Within six hours of emergence, workers accurately find and eat all of the diploid males (Woyke 1963, 1965b, 1967). V: Sexual Selection Darwin clearly thought of sexual selection as a logical but milder extension of natural selection such that the least healthy and vigourous of the extant excess population are reproductively culled by group-internalized selection criteria (Darwin 1859 p. 94, 1874 p. 226). Darwin (1874 Preface) rejected all claims that he "invented" sexual selection to cover those features of organisms that were said to be inexplicable or appeared maladaptive. The first published exposition of the hypothesis appears in Darwin (1859 Chapter 4) as an adjunct to the central theme of the chapter. Darwin's primary criterion of sexual selection was demonstrable vigour and, only secondarily, attractiveness (1874 pp. 213-215, 405, 595, 616). Fisher (1930) algebraically inverted the argument, emphasizing selection for attractiveness, thereby mathematically isolating attractive traits from the genome as a whole, leading to the theoretical phenomena of "runaway" selection and non-optimal disunity in the evolved genome. The mathematics of modern sexual selection theory has been predominately Fisherian in its orientation.
I sincerely thank Alex Mangini, Naida Zucker, Richard Spellenberg, James Zimmerman, Ralph Raitt, Stuart Pimm, Graham Bell, Jorge Zeballos, Peter Jewell, Yutaka Saito and an anonymous reviewer for their thoughtful comments and discussions on this subject. Thanks are especially due Valerie Atmar, James H. Brown, Andrew Price and Bruce D. Patterson, not only for their encouragement, but also for their time and their critical comments. This paper is dedicated to Ralph Raitt, on the occasion of his retirement from teaching, with much appreciation.
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