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INFLUENCE OF
BEHAVIORAL, ECOLOGICAL, AND
PHYSIOLOGICAL FACTORS ON THE SEX RATIO
Of Arthropods
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Overview 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. Considerable changes occurred in the sex ratios of several pteromalid species
that were subjected to various types of ovipositional restraint (Legner &
Gerling 1967 ). 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%. Physiological Phenomena 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) Muscidifurax (pteromalid)--Legner (1969a , 1987a, 1987b), Kogan & Legner (1970), Stouthamer et
al. (1990) 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 which 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
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