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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) 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
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