INFLUENCE OF BEHAVIORAL, ECOLOGICAL, AND
PHYSIOLOGICAL FACTORS ON THE SEX RATIO
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A number of factors directly or indirectly affect the gonads and differential survival of the developing female and male which determine the sex ratio. Included are the topographical environment, larval competition, extremes in temperature, behavior, nutrition, selective breeding, physiological phenomena (ovisorption, spermathecal gland), mating, the age of the male and female, and delayed and interrupted oviposition.
Clausen (1940) emphasized that the sex ratio in parasitic Hymenoptera is variable with the following: the sex ratio of the host, successive generations of the same or a different host generation, different hosts, upon the same host in the same season but in different geographical regions, and in successive years when the host is increasing or decreasing rapidly.
Behavioral and Ecological Phenomena
Effects of the Topographical Environment.--It was reported by S. G. Smith (1941) that the uniparental form of Diprion polytomum in Canada appeared to consist of strains differing in the frequency of male production. Since then there has been much circumstantial evidence for the production of males from thelytokous populations following periods of hot weather (temperatures above 32BC). Earlier and contemporary examples are found in the mymarid, Anagrus spp. and Paranagrus spp. (Perkins 1905); a sawfly, Diprion polytomum (Smith 1941); and the chalcids, Harmolita grandis (Phillips & Emery 1919, Phillips 1920), Habrolepis rouxi (Flanders 1945), and Ditropinotus aureoviridis (Phillips & Poos 1921).
A more recent study in the West Indies showed that Muscidifurax raptor Girault & Sanders is characteristically biparental (20% males) at sea level in Puerto Rico and uniparental (M. uniraptor Kogan & Legner sibling) above 3,000 ft. (Legner, Bay & White 1967). A study of this complex offers proof that temperature may influence speciation in Hymenoptera.
Effects of Larval Competition.--Salt (1936) reported that Trichogramma male larvae have a better advantage in survival than females. However, Jenni (1951) found the opposite where female larvae of Pseudeucoila have the competitive advantage. Wilkes (1963) showed that a mutant strain of Dahlbominus fuliginosus produced female larvae that outcompeted male larvae, although the normal strain followed the usual pattern of male larvae having the advantage.
In multiple parasitism, the individual present first usually survives. Grosch (1948) showed increased larval mortality involving the female more than the male; and Wheeler (1911) and Vandel (1932) showed the same response in Strepsiptera. All these examples were with gregarious species.
Superparasitism and subsequent larval competition was found to reduce the percentage of female progeny from 73.6% to 9.8% in Bracon gelechiae (Narayanan & Rao 1955), and Bracon hebetor Say from 50% to 26.4% (Kanungo 1955). Superparasitism by Macrocentrus under mass culture conditions tends to increase the proportion of females (Finney et al. 1947).
Effects of Humidity and Light Intensity.--Humidity and light are thought to affect the sex ratio by interfering with the larval stage that loses in competition. Mating patterns are also thought to be affected which in turn changes the sex ratio in a population (Flanders 1946).
Effect of Host Size.--The size of the host determines the sex ratio in gregarious Hymenoptera, the proportion of males in a population being higher with small hosts (Chewyrew 1912, Holdaway & Smith 1932, Seyrig 1935, Taylor 1937, Ullyett 1936).
Wilkes (1963) found no preferential deposition of fertilized eggs in large cocoons of sawflies by Dahlbominus. He thought that all sex ratio differences in this species were a result of differential survival of sexes among larvae.
In Macrocentrus, the rate of oviposition was determined by host size, which influenced the sex ratio (Finney et al. 1947).
In Pteromalus coloradensis (Ashmead), morphometric analysis of individual host puparia and parasitoids showed three distinct relationships between size and sex of the parasitoid to the size of the host puparium, thereby substantiating predetermination of sex by the ovipositing female (Headrick & Goeden 1989)
In some species of Pteromalidae and Diapriidae, parasitoids of house flies, a greater fertilized egg deposition occurred on large hosts of the same species by parasitoids that were adapted to large hosts (solitary species). Parasitioids adapted to small hosts (e.g., Spalangia drosophilae) produced more fertilized offspring from small hosts (Legner 1969b).
Effects of Host Availability.--In Prospaltella spp. and Encarsia spp., the sex ratio depends on the ratio of host moth eggs (which produce males) and coccid nymphs and adults (which produce females) (Flanders 1959).
Effects of Host-Parasitoid Density.--The percentage of female Nasonia vitripennis decreased as the proportion of female parasitoids increased (i.e., ovipositing parents). Superparasitism was increased and several mechanisms were postulated (Wylie 1965c, 1966): (1) an increased mortality of female larvae, (2) a smaller percentage of eggs might have been fertilized due to interference among females, and (3) a smaller percentage of eggs might have been fertilized due to more frequent contacts with previously pierced pupae. However, this contributes only a small portion of the observed female reduction because female eggs laid on previously pierced hosts are only about 20% less than on unattacked hosts.
Nasonia vitripennis apparently can restrain egg fertilization by detection with the ovipositor changes that occur in the hosts after they are pierced in a previous attack (Wylie 1965a). Changes are thought to be physical (heart beat stop) or chemical (the injection of a venom). A conservation of immature larvae and sperm results because eggs are not fertilized under conditions of superparasitism. Therefore, resultant male larvae are more capable of completing their development than female larvae.
Behavior.--There is a distinct correlation between the degree of restraint in oviposition and the preponderance of female progeny (Flanders 1939). This is especially characteristic in the Serphoidea (Clausen 1940) in which most endoparasitic species are hydropic.
Mating.--Flanders (1946a) reported that multiple matings in Macrocentrus ancylivorus Rohwer, resulted in the crowding of spermatophores in the vagina which prevented any of them from making contact with the sperm duct opening, and thus passage of the sperm to the sperm receptacle was barred. This negative effect of matings is probably limited to species which transfer a spermatophore.
It was found that Dahlbominus fuliginosus (Nees) females rarely mated more than once. When they did, sperm from the second mating was sometimes used. Therefore, a single female who mated with two males could give rise to some daughters with characteristics of one father and other daughters with characteristics of the other father (Wilkes 1963). However, the sex ratio among the progeny suggested that the sperm already in the spermatheca takes precedence over sperm from subsequent matings. How this comes about is obscure since all sperm from first and second matings are thoroughly mixed. Wilkes performed his experiment with genetic markers. His particular mutant showed a switch in the strength of female larvae so that they won out in competition more often than males. It seems as if the employment of genetic markers in this case posed more problems than solutions.
Delayed and Interrupted Oviposition.--Delaying and interrupting oviposition can result in a female progeny reduction. This was shown by Wilkes (1963) and Legner & Gerling (1967 ).
Heteronomous Parasitoids.--This group includes those species where males and females have different hosts or feed on the same host but in different ways. Heteronomous parasitoids occur in eight genera of Aphelinidae: Aneristus, Coccophagus, Euxanthellus, Prococcophagus, Lounsburia, Physcus, Coccophagoides and Encarsia. Walter (1983) reported on a series of unusual male ontogenies in these genera. Well known cases involve heteronomous hyperparasitism in which females are primary endoparasitoids, while males are hyperparasitoids developing either on a larva or pupa of their own species (usually a female), or of another internal parasitoid. The sex ratio in such wasps is not only determined by the decision of a female to fertilize her eggs, but is constrained by the availability of suitable hosts for either male or female offspring. Females of Encarsia pergandiella oviposit male or female eggs in a manner that is not directly related to the abundance of suitable hosts, but rather prefer to hyperparasitize and lay male eggs. Although they may show a preference to hyperparasitize, the ratio of suitable hosts encountered in nature will generally favor unparasitized hosts, leading to female biased sex ratios (Neuffer 1964, Smith et al. 1964).
Theoretical Considerations.--Although adaptive sex ratios in outcrossed vertebrates seem to favor a Mendelian or random binomial sex determination mechanism (Williams 1979), it was proposed by Green et al. (1982) that because parasitic wasps possess a mechanism for regulating the sex of their progeny (namely arrhenotoky), they show deviations from random sex determination. Sex ratios may vary with host size in outcrossed wasps (Charnov 1979, Charnov et al. 1981), but highly inbred wasps are thought to have highly female-biased sex ratios (Hamilton 1967). Green et al. (1982) showed strong tendencies toward preciseness of sex ratios in bethylids; and Legner & Warkentin (1988 ) supported the general trend of bethylids to precise sex ratios, except that host-parasitoid density interactions may skew sex ratios within a small range of approximately 10%.
Temperature.--Cases of the occurrence of thelytokous stocks of a species have been known for decades; and changes in temperature (usually to a higher temperature) have been observed to produce males in these populations. A few well known cases of thelytokous forms of a species are the following:
Gilpina polytoma (sawfly)--Balch et al. (1941)
Ephialtes extensor (ichneumonid)--Rosenberg (1934)
Lysiphlebus tritici (braconid)--Webster (1909)
Habrobracon juglandis (braconid)--Whiting (1924)
Pteromalus puparum (pteromalid)--cited by Adler (Howard 1891)
Atta cephalotes (formicid)--Wheeler (1928)
Lasius niger (formicid)--Crawley (1912)
Campomeris trifasciata (vespid)--Box (1925)
Apis mellifera (honeybee)--Onion (1912, 1914), Jack (1917), Makenson (1943)
Trichogramma (trichogrammatid)--Bowen & Stern (1966)
High Temperatures. --Males are produced in the thelytokous chalcid, Habrolepis rouxi, by treating larval females to 90BF (32.2BC) (Flanders 1945). A thelytokous form of Ooencyrtus submetallicus (Howard) began male production through heat treatment (Wilson & Woolcock 1960). A population of the encyrtid, Pauridia peregrina Timberlake that normally reproduced uniparentally (by thelytoky) gave rise to an arrhenotokous generation through heat treatment (Flanders 1965). Moursi (1946) produced one female that reproduced by thelytoky by treating all developmental stages to 27.5BC. Bowen & Stern (1966) discussed the wide distribution of Trichogramma semifumatum (Perkins) as an arrhenotokous population in the southwestern United States. One thelytokous (deuterotokous cited) form was found in Bishop, California on vegetation near the base of the Sierra Nevada Mountains.
The Bowen & Stern (1966) experiments showed that temperatures above 85BF (30BC) caused a progressively increasing mortality of female adults exposed. A critical period of only a few hours existed during the time that the oogonia were forming in the female pupa. The sex of the progeny could be changed to mosaics (a small percentage) and finally males if heat treatment occurred during the critical period. All males were thought to be sterile as they did not successfully inseminate females of the arrhenotokous form so that female progeny could be produced.
Quezada (1967) secured males in a thelytokous Signiphora species, a parasitoid of coconut scale, Aspidiotus destructor Signoret, by treatment of newly formed parasitoid pupae to 90BF for 48 hrs. Oogenesis continued through the pupal stage and into young adults. Quezada could not imagine why similar treatment with heat did not affect parthenogenesis in some later developmental stages.
In Muscidifurax uniraptor, which reproduces naturally by thelytoky, a production of excess males was triggered by high temperature (32.2°C) during oviposition, and was thought to result from a blockage of endomitosis in the egg (Legner 1985b). A minimum oviposition period of 24-h at 25°C prior to continuous high temperature was an important prerequisite. A few receptive oocytes were thought to be present before oviposition, with new ones formed during the first 24-h of the oviposition period at 25°C. Although heat treatment had to begin during a relatively short receptive period ("window of susceptibility") early in adult life, it had to persist longer than 24-h at low oviposition rates and <24-h at high oviposition rates to block effectively endomitosis and the formation of diploid, female-producing eggs (Legner 1985b). The males produced have a very low sperm viability, but can inseminate females of M. raptor on occasion. The effect of temperature is positive even through the second cleavage stage! (Legner 1985a, 1985b; 1987a). Results in the laboratory show that both high and low temperatures can influence this kind of reproduction.
Wilkes (1959) found that high temperatures had a much greater influence on the sex ratio of the arrhenotokous Dahlbominus fuliginosus (Nees) because of sterilizing effects during post embryonic development. At high temperatures a far greater proportion of females survive than males. Of those individuals surviving, sterilization is much higher in the males. For example, males are sterilized at 27BC and females at 30BC, when exposed as larvae.
Low Temperatures. --Schread & Garman (1933, 1934) showed a sex ratio upset in Trichogramma stored at 47BF (8.3BC). Lund (1938) found that females that had developed at about 15BC (59BF) and then oviposited at 25BC (77BF) produced more males than females. Anderson (1935) and van Steenburgh (1934) observed that the fertility of parasitoids subjected to low temperatures during development may be adversely affected. Supposedly healthy mature parasitoids, therefore, may in fact be more or less impotent. Euchalcidia caryobori Hanna larvae stored at 60BF (15.6BC) showed no subsequent disturbance in sex ratio of their offspring. However, then pupae are stored at this temperature, a preponderance of male progeny resulted (Hanna 1935). This was interpreted as a sterilization of males at the low temperatures.
Nasonia vitripennis larvae stored at near freezing temperatures sustain a greater mortality of males, causing a predominant female sex ratio (DeBach 1943). DeBach & Rao (1968) found that eight hours at 30BF (-1.1BC) was lethal to Aphytis sperm. Moursi (1946) reviewed a number of cases where low temperatures especially seemed to produce sex ratio changes. He thought the effects might have been manifested by the following: (1) inadequate stimulation of the spermathecal gland, (2) depletion of spermathecal secretions and (3) failure of spermathecal nerves and muscles to function or synchronize the discharge of sperm with the expulsion of eggs through the oviduct. Flanders (1938) suggested that male sterility in Tetrastichus resulted from gonad malnutrition in mature larvae and pupae. This was caused by prolonged exposure to low nonlethal temperatures. Solitary third instar Spalangia drosophilae larvae when stored at low temperatures (7 & 11BC), gave rise to adults with changed fecundities; and these produced a preponderance of female progeny (Legner 1967a). Tropical races of this parasitoid suffered a loss in longevity and fecundity. However, prolonged storage of mature larvae of Muscidifurax raptor, M. zaraptor and Spalangia endius at 10BC (50BF) did not influence the sex ratio of surviving adults (Legner 1976). Uvarov (1931) stated that the development of gonads may be seriously inhibited by temperature which can hardly be called low in the normal sense of the word. He referred to work which was later reported by Hanna (1935) who worked with a tropical species of Euchalcidia caryobori Hanna.
Differential temperature thresholds exist for oviposition and sperm activation in Formica rufa. Oviposition occurs, but sperm are not activated below 15.5BC. Progeny below this temperature are, therefore, all males (Grosswald & Bier 1955).
Nutritional Influences. --In the uniparental braconid Microctonus brevicollis parasitic on a beetle in Algeria, all females are produced when oviposition occurs in beetle larvae. Some males are produced when eggs are laid in adult beetles, with males emerging in the spring (Kunckel et al. 1891). Various species of sawflies feeding on alder are to a great extent unisexual while very closely related species feeding on birch are bisexual (van Rossum, as reported by Bischoff 1927). The chalcid, Prospaltella perniciosi Tower, is bisexual when reproducing on San Jose scale growing on peach trees, and unisexual when reproducing on San Jose scale growing on the cow melon, Citruilus vulgaris, in the laboratory (Flanders 1944). Also, the gall forming eurytomid, Trichilogaster acaciae longifoliae is unisexual on one variety of Acacia and bisexual on another variety (Flanders 1945).
In Muscidifurax uniraptor aged females produce more adventitious males than younger females, which may be a nutritional phenomenon (Legner & Gerling 1967 ). Recent studies of four thelytokous Puerto Rican isolates this species revealed the existence of four behaviorally distinct strains that differed initially in diapause and nondiapause emergence, and the age when female progeny were produced. Subsequent F1 and F2 progeny differed in sex ratio and total progeny production (Legner 1988). Mating F2 females from nondiapause isolates to naturally emerging males from thelytokous populations significantly reduced total progeny and the proportion of females to ca. 20%. These mated females at first resembled in behavior those which originated from diapausing parents. Random mating within all isolates beginning in the F1, resulted in a general lower survival and progeny production but was accompanied by a rise in sex ratio to ca. 50% female by the F6 generation (Legner 1988). Although the interinvolvement of extranuclear and genic factors were considered, nutritional phenomena might partially explain these observations.
The inability of the male larva of Pimpla turionellae L. to consume enough food in large hosts to make such hosts suitable for male pupation, increases the proportion of females.
In species that reproduce uniparentally such as Encarsia formosa Gahan, all or most of the primary oogonia may be tetraploid. This is also indicated in Habrolepis rouxi Compere. The sex ratio of the progeny is apparently determined by the quality of nutrient material that the parent female ingests during her late embryonic and early larval stages. The effect of the abnormal nutrient condition during the early developmental stages of the primary oogonia is more likely to have an immediate effect such as halving of the chromosome number to diploid from tetraploid, than it is to have a delayed effect such as preserving the diploid number at maturation (Flanders 1956).
Age.--Older females produce relatively fewer female progeny than younger females (Wilkes 1963, Legner & Gerling 1967 ). Mating response changes with age (Crandell 1939).
Photoperiod. --In Pteromalus puparum (Bouletreau 1976) and Campoletis perdisticus (Hoelscher & Vinson 1971) the photoperiod significantly influences the sex ratio by causing a greater percentage of female offspring to be produced in a 10:14 LD in the former and a 12:12 LD for the latter.
Selective Breeding. --Simmonds (1947) increased the percentage of females in a laboratory culture of Aenoplex carpocapsae (Cushman) that was reared on field-gathered larvae of Carpocapsa pomonella (L>) by propagating only males and females whose mothers gave rise to the greatest number of female progeny. It was concluded that when selective matings are made so that individuals are chosen from families showing a high female sex ratio, a strain can be bred in which the sex ratio is increased due to the breeding out of factors inducing male sterility. Male sterility as used by both Simmonds and Wilkes is a misnomer, because it is based on the fact that mated females did not produce female progeny. Females well supplied with viable sperm may use non although depositing the normal number of eggs (Flanders observed this in three mated Macrocentrus females). Other factors that might produce the same effect are associated with anatomical or physiological peculiarities of the female spermatheca. Still other causes might be genetic. Simmonds got his desired effect after the 6th and 7th generations.
Wilkes (1947) reduced male sterility to about 2% by selective breeding in Microplectron fuscipennis Zett., parasitoid introduced in Canada from Europe to control European spruce sawfly, Gilpinia hercyniae Htg. Wilkes got his effect after 8-10 generations.
Through selection it was possible to lower the sex ratio in the eulophid Dahlbominus fuliginosis from a normal 92% females to about 5% females (Wilkes 1964). From crossing experiments between the low and the normal sex-ratio lines, it appeared that low sex ratio traits appear to be genetic and only are expressed in males. Males from the low sex ratio line produced few female offspring when crossed with normal females and females from the low sex ratio line produced normal sex ratios when crossed with males from the normal sex ratio line. The cause of this low sex ratio appeared to be the low number of successfully fertilized eggs. Later Lee & Wilkes (1965) and Wilkes & Lee (1965) discovered that males of the normal sex ratio strain of Dahlbominus produced two main types of sperm that differed in the direction of the helix on the sperm head. The proportions of a dextral oriented type was 38% in the spermatheca of females inseminated by the low sex ratio males, whereas it was 70% in spermathecae of females inseminated by normal males. Wilkes & Lee (1965) presented evidence that the sinistrally coiled sperm were not able to penetrate the vitelline membrane of the egg, thus leaving the fertilized egg functionally haploid.
Parker & Orzack (1985) produced a significant decline in the sex ratio of Nasonia from 80-90% female in an unselected line to 50-55% female in a line selected for low sex ratio. In this case the low sex ratio was due to females fertilizing fewer of their eggs.
Luck et al. (1996) mention an often quoted case of selection for high sex ratio in the ichneumonid Aenoplex carpocapsae (Simmonds 1947). In laboratory rearings started with only six females and five males, the sex ratio declined over a few generations from about 50% to about 13%. In the subsequent generations Simmonds (1947) was able to raise the sex ratio to the range of 26-39% by crossing individuals from high sex ratio families. However, the next generation the population became extinct. The cause of the increase in sex ratio in this case may not be inheritable but simply the result of creating heterozygosity counteracting the negative effects of inbreeding on the sex ratio.
Few studies have determined the effects of inbreeding on the sex ratio of Hymenoptera. The effects of inbreeding Muscidifurax raptor were determined (Fabritius 1984). Inbred lines were begun by taking four sibmated females from a four-year old laboratory culture. Per generation only four pairs were used, all consisting of the offspring of one mother of the previous generation. No effects due to inbreeding were noted. Although the sex ratio declined over time, the variance in sex ratio per generation suggested that this decline was not significant. Over the generations the fecundity of the pairs declined significantly until in the 47th generation the pair did not produce any offspring. Five generations of sibmatings in Leptopilina heterotoma (Hey & Garglulo 1985) did not lead to changes in sex ratio. Inbreeding did seem to affect the time when female eggs were laid, however. Inbred females laid female offspring earlier than outbred females.
Microorganisms. --Extrachromosomal factors in the form of microorganisms (e.g., viruses, bacteria, spiroplasmas) can alter sex ratios in parasitoids by selectively killing developing males or females (Skinner 1982, 1985; Vinson & Stoltz 1986, Werren et al. 1981, 1986). Stoltz & Vinson (1977) and Stoltz et al. (1976) have found viruses in the calyx epithelial cells of endoparasitoids; and Fleming and Summer (1986) found them also in the lumen of the oviduct. These viruses were passed from parent to offspring, males being able to transmit viral DNA to females with whom they mated (Stoltz et al. 1986). Generally if males carry a particular sex ratio factor this will cause the females they mate with to produce males, while if females care the carriers the sex ratio will be skewed toward females (Werren 1987, Cosmides & Tooby 1981).
In Hymenoptera microorganisms or yeasts are found in the ovaries of many species, often without obvious effects on their hosts (Byers & Wilkes 1970, King & Radcliffe 1969, Kurihara et al. 1982, Middeldorf & Ruthmann 1984, LeBeck 1985). Intensive studies of Nasonia vitripennis have revealed at least three different extrachromosomal factors that distort the sex ratio, indicating that such may also be found in other Hymenoptera.
In the maternal sex ratio factor, msr, found in Nasonia (Skinner 1982), females carrying it produce male offspring only when they are virgins, after mating practically all their offspring are female. This factor has a strictly maternal inheritance which would be consistent with a microorganism. However, the exact nature is yet unknown. Similarly virgin females of Coccophagus lyciminia produce only male offspring, while mated females produce only female offspring (Flanders 1943); however, neither the cause nor the mode of inheritance of this trait are known.
The sonkiller trait (sk) of Skinner (1985), also found in Nasonia, is caused by a rod shaped bacterium (Werren et al. 1986). Infection with this bacterium leads to the death of male offspring in the larval stage, but does not kill females. This bacterium infects many different tissues, and transmission from mother to offspring takes place probably through the haemolymph of the parasitized host (Huger et al. 1985). In Hymenoptera no other confirmed cases of son killing bacteria are known; however, the symptoms described by Jackson (1958) in a strain of Caraphractus cinctus are consistent with a son killing bacteria. Virgin females of a low sex ratio strain produced very few male offspring, about 3% of what the normal strain would produce, and mated females from both normal and sex ratio strains produced similar numbers of females. Sex ratio distortion, in which only the male sex dies, is known from many nonhymenopteran insect species, but other causal factors may be involved. For example in some species of the Drosophila willistoni group, spiroplasmas, or their associated viruses, are the causal agent of a sex ratio condition. Such a condition is also known from various Coccinellidae (Gotoh 1982, Gotoh & Niijima 1986, Kai 1979, Matsuka et al. 1975), but the causal agent is unknown.
A non-reciprocal cross incompatibility (NRCI) has been found which is evident in crosses between strains, one carrying a particular microorganism (Wolbachiae) and another which is not. Eggs containing these microorganisms are compatible with sperm from both infected and uninfected males, whereas eggs free of microorganisms can only be successfully fertilized by sperm from mates free of microorganisms. This trait results in all male offspring in the cross between males not carrying and in females carrying the organisms, whereas the reciprocal cross results in offspring with a normal sex ratio. In Hymenoptera this trait has only been found in Nasonia. Transmission appears to be entirely through the maternal line (Saul 1961). But, this trait can be acquired by the wasps in laboratory cultures (Conner & Saul 1986), possibly through their hosts. The incompatibility can be removed by antibiotic treatment (Richardson et al. 1987). In other species of Hymenoptera (Pseudocoila bochi--Veerkamp 1980), Aphidius ervi and A. pulcher (Mackauer 1969) and several Trichogramma spp. (Nagarkatti & Fazaluddin 1973, Pintureau 1987), similar incompatibilities are found but the cause of the NRCI has not been determined. In Trichogramma deion NRCI between two strains appears not to be caused by microorganisms with a purely maternal inheritance but rather by nuclear genes (Stouthamer 1989). An apparent microbe induced incompatibility in many other insect species: Culex (Laven 1957, Yen & Barr 1973), Aedes (Wright & Wang 1980), alfalfa weevil, Hypera postica (Hsiao & Hsiao 1985), flour beetle, Tribolium (Wade & Stevens 1985), grainmoth, Ephestia cautella (Kellen et al. 1981), fruit flies Drosophila (Hoffmann 1988).
Little is known about the influence of the microorganisms on the longevity and fecundity of Nasonia nor other species. Awahmukalah & Brooks (1983, 1985) reported that aposymbiotic females of an inbred strain of Culex pipiens L. have a much reduced productivity, and hypothesized that the Wolbachiae supply essential nutrients to its host. This contrasts with Ephestia (Kellen et al. 1981) where the microbes do not have any influence on fecundity. Aposymbiotic Drosophila simulans have a higher offspring production than infected females, however (Hoffman & Turelli 1988).
The manner in which uniparental (thelytokous) reproduction was incorporated in a hybrid biparental (arrhenotokous) population of Muscidifurax raptor Girault & Sanders after mating with males of thelytokous Muscidifurax uniraptor Kogan & Legner implicated extranuclear factors; e.g. microorganisms and chemical substances (Legner 1987b). It was thought that genetic change may not only be involved in the acquisition of thelytoky.
Stouthamer et al. (1990) found that completely parthenogenetic Trichogramma wasps could be rendered permanently bisexual by treatment with three different antibiotics or high temperatures. The evidence suggested that maternally inherited microorganisms cause parthenogenesis in these wasps.
Paternal Sex Ratio. --The paternal sex ratio (psr) element (Werren et al. 1981) is of chromosomal origin (Werren et al. 1987) and is found in Nasonia vitripennis. Males carrying this element cause the females they mate with to produce only male offspring. Sperm-carrying psr will fertilize an egg, but subsequently the paternal genome condenses and forms a dense mass. The psr element itself is transmitted intact and the fertilized egg therefore carries the maternal (haploid) set of chromosomes plus the psr element from the male. Such an egg will give rise to male offspring carrying psr. When these males mate again with females only the psr factor will be inherited by the male offspring of such fertilized eggs. Within a population the dynamics of the psr factor are largely determined by the percentage fertilization, as long as this percentage is less than 50% the factor is believed to decrease in frequency.
Exercise 20.1--How may the sex ratio be influenced in parasitic Hymenoptera?
Exercise 20.2--Discuss the effects of high temperatures on thelytokous populations.
Exercise 20.3--Describe how selective breeding can result in the production of a greater proportion of females. Discuss the advantages of this, if any.
Exercise 20.4--Make a list of the usual sex ratios found in nature among predatory and parasitic arthropods.
Exercise 20.5--Discuss sex ratio changes in parasitoids that reproduce by thelytoky.
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