Inherited sterility in insects
Encyclopedia
Inherited sterility in insects is induced by substerilizing doses of ionizing radiation. When partially sterile males mate with wild females, the radiation-induced deleterious effects are inherited by the F1 generation. As a result, egg hatch is reduced and the resulting offspring are both highly sterile and predominately male. Compared with the high radiation required to achieve full sterility in Lepidoptera, the lower dose of radiation used to induce F1 sterility increases the quality and competitiveness of the released insects as measured by improved dispersal after release, increased mating ability, and superior sperm competition.
(SIT) as a component have been successful against a number of pest flies or Diptera such as the New World screwworm, Cochliomyia hominivorax
, various species of tephritidae
fruit flies and against tsetse flies (Glossinidae). However, most moths
or lepidopterans are more resistant to radiation than dipterans, and as a consequence, the higher dose of radiation required to completely sterilize lepidopterans reduces their performance in the field. One approach to circumvent the negative effects associated with the high radio-resistance of Lepidoptera
pests has been the use of inherited sterility or F1 sterility, first documented in studies on the codling moth
(Cydia pomonella). Inherited sterility has also been documented in the Hemiptera
order.
The silk worm Bombyx mori
(Lepidoptera: Bombycidae
) was the fist insect in which inherited sterility was reported. Then inherited sterility was reported in the greater wax moth Galleria mellonella
(Lepidoptera:Pyralidae
), in the codling moth Cydia pomonella (Lepidoptera: Tortricidae
), in the large milkweed bug Oncopeltus fasciatus
(Hemiptera: Lygaeidae), in Gonocerus acuteangulatus (Hemiptera: Coreida), in Rhodnius prolixus
(Hemiptera: Reduviidae
), and in the Two-spotted spider mite Tetranychus urticae
(Acari: Tetranychidae).
s cause lethality in Diptera in the developing zygote are well documented,,. The primary lesion leading to a dominant lethal mutation is a break in the chromosome, in this case, induced by radiation. When a break is induced in a chromosome in mature sperm, it remains in this condition until after the sperm has entered an egg. Following fusion, nuclear divisions begin, and a break in a chromosome can have drastic effects on the viability of the embryo as development proceeds. During early prophase
the broken chromosome undergoes normal replication, but during metaphase
the broken ends can fuse leading to the formation of a dicentric chromosome and an acentric fragment. The acentric fragment is frequently lost, while the dicentric fragment forms a bridge at anaphase
leading to another chromosomal break. This whole process then repeats itself, leading to the accumulation of serious imbalances in the genetic information of the daughter cells. The accumulation of this genetic damage finally leads to the death of the zygote (Fig. 1).
Diptera, Hymenoptera, and Coleoptera orders can be classed as radiation-sensitive, while Lepidoptera, Homoptera and mites (Acari) orders are radiation-resistant. A major difference between these two groups of Insects is that the former group has a localized centromere
(monokinetic), while the latter has a diffuse centromere (holokinetic),,,. However, more recent work suggested that lepidopteran chromosomes are intermediate between holokinetic and monocentric chromosomes. In any case, the centromere difference is believed to play a major, although not exclusive, role in radiation sensitivity. It was suggested, that possible molecular mechanisms responsible for the high radioresistance in Lepidoptera might include an inducible cell recovery system and a DNA repair probes.
Lepidoptera also do not show the classical breakage-fusion-bridge cycle that is a characteristic of dominant lethals induced in Diptera (Fig. 1). It appears that lepidopteran chromosomes can tolerate telomere loss without the drastic effects that this has on chromosomes in other orders. Lepidopteran chromosomes possess a localized kinetochore
plate to which the spindle microtubules attach during cell division. The kinetochore plates are large and cover a significant portion of the chromosome length, ensuring that more radiation-induced breaks will not lead to the loss of chromosome fragments as is typical in species with monocentric chromosomes. In species with large kinetochore plates, the fragments may persist for a number of mitotic cell divisions, and can even be transmitted through germ cells to the next generation. The plates also reduce the risk of lethality caused by the formation of dicentric chromosomes, acentric fragments, and other unstable aberrations.
Field programmes releasing irradiated moths under an SIT or inherited sterility approach have been in operation since the 1960s. The pink bollworm, Pectinophora gossypiella has been successfully contained since 1969 in cotton areas of the San Joaquin Valley in California and is being successfully targeted for eradication from cotton areas in the south-western USA and north-western Mexico. Since the early 1990s, the codling moth has been successfully suppressed in apple and pear production areas in the Okanagan Valley in British Columbia, Canada, and countries such as Argentina, Brazil and South Africa have plans or programmes against this pest. New Zealand eradicated outbreaks of the Australian painted apple moth, Teia anartoides. Mexico eradicated outbreaks of the cactus moth, Cactoblastis cactorum and the USA contains its advance along the Gulf of Mexico coast. South Africa has a programme to suppress the false codling moth, Thaumatotibia leucotreta in citrus orchards
Control of most moth pests is hampered by the increased resistance to the most widely used broad spectrum insecticides; hence the potential for expanded implementation of inherited sterility as part of an area-wide integrated approach is considerable.
History of Inherited Sterility
Area-wide integrated pest management programmes using the sterile insect techniqueSterile insect technique
The sterile insect technique is a method of biological control, whereby overwhelming numbers of sterile insects are released. The released insects are normally male as it is the female that causes the damage, usually by laying eggs in the crop, or, in the case of mosquitoes, taking a bloodmeal from...
(SIT) as a component have been successful against a number of pest flies or Diptera such as the New World screwworm, Cochliomyia hominivorax
Cochliomyia hominivorax
Cochliomyia hominivorax, the New World screw-worm fly, or screw-worm for short, is a species of parasitic fly that is well known for the way in which its larvae eat the living tissue of warm-blooded animals. It is present in the New World tropics...
, various species of tephritidae
Tephritidae
Tephritidae is one of two fly families referred to as "fruit flies", the other family being Drosophilidae. Tephritidae does not include the biological model organisms of the genus Drosophila , which is often called the "common fruit fly". There are nearly 5,000 described species of tephritid...
fruit flies and against tsetse flies (Glossinidae). However, most moths
Moths
Moths may refer to:* Gustav Moths , German rower* The Moths!, an English indie rock band* MOTHS, members of the Memorable Order of Tin Hats...
or lepidopterans are more resistant to radiation than dipterans, and as a consequence, the higher dose of radiation required to completely sterilize lepidopterans reduces their performance in the field. One approach to circumvent the negative effects associated with the high radio-resistance of Lepidoptera
Lepidoptera
Lepidoptera is a large order of insects that includes moths and butterflies . It is one of the most widespread and widely recognizable insect orders in the world, encompassing moths and the three superfamilies of butterflies, skipper butterflies, and moth-butterflies...
pests has been the use of inherited sterility or F1 sterility, first documented in studies on the codling moth
Codling moth
The codling moth is a member of the Lepidopteran family Tortricidae. They are known as an agricultural pest, their larva being the common apple worm or maggot. It is native to Europe and was introduced to North America, where it has become one of the regular pests of apple orchards. It is found...
(Cydia pomonella). Inherited sterility has also been documented in the Hemiptera
Hemiptera
Hemiptera is an order of insects most often known as the true bugs , comprising around 50,000–80,000 species of cicadas, aphids, planthoppers, leafhoppers, shield bugs, and others...
order.
The silk worm Bombyx mori
Bombyx mori
The silkworm is the larva or caterpillar of the domesticated silkmoth, Bombyx mori . It is an economically important insect, being a primary producer of silk...
(Lepidoptera: Bombycidae
Bombycidae
Bombycidae is a family of moths. The best-known species is Bombyx mori or silkworm, native to northern China and domesticated for millennia...
) was the fist insect in which inherited sterility was reported. Then inherited sterility was reported in the greater wax moth Galleria mellonella
Galleria mellonella
The Greater Wax Moth or Honeycomb Moth is a moth of the family Pyralidae. It is the only member of the genus Galleria. It is found in most of the world, including Europe and adjacent Eurasia , and as an introduced species e.g...
(Lepidoptera:Pyralidae
Pyralidae
The Pyralidae or snout moths are a family of Lepidoptera in the ditrysian superfamily Pyraloidea. In many classifications, the grass moths are included in the Pyralidae as a subfamily, making the combined group one of the largest families in the Lepidoptera...
), in the codling moth Cydia pomonella (Lepidoptera: Tortricidae
Tortricidae
Tortricidae is a family of moths, commonly known as tortrix moths, in the order Lepidoptera. Tortricidae is a large family with over 9,400 species described, and is the sole member of the superfamily Tortricoidea. Many of these are economically important pests. Olethreutidae is a junior synonym...
), in the large milkweed bug Oncopeltus fasciatus
Oncopeltus fasciatus
The milkweed bug, Oncopeltus fasciatus, is a medium–sized hemipteran of the family Lygaeidae. It feeds mainly on grains, particularly those of the milkweed. Like all hemiptera, it feeds through a long mouthpart known as a rostrum. O...
(Hemiptera: Lygaeidae), in Gonocerus acuteangulatus (Hemiptera: Coreida), in Rhodnius prolixus
Rhodnius prolixus
Rhodnius prolixus is the second most important triatomine vector of the Chagas parasite due to its efficient adaptation to the human domicile in northern South America, where sylvatic populations also exist, and in Central America where it is exclusively domestic...
(Hemiptera: Reduviidae
Reduviidae
Reduviidae is a large, cosmopolitan family of predatory insects in the suborder Heteroptera...
), and in the Two-spotted spider mite Tetranychus urticae
Tetranychus urticae
Tetranychus urticae is one of many species of plant-feeding mites found in dry environments across the world, and generally considered a pest. It is the most widely known member of the family Tetranychidae or spider mites...
(Acari: Tetranychidae).
Genetic Basis of Inherited Sterility
The mechanisms by which mutationMutation
In molecular biology and genetics, mutations are changes in a genomic sequence: the DNA sequence of a cell's genome or the DNA or RNA sequence of a virus. They can be defined as sudden and spontaneous changes in the cell. Mutations are caused by radiation, viruses, transposons and mutagenic...
s cause lethality in Diptera in the developing zygote are well documented,,. The primary lesion leading to a dominant lethal mutation is a break in the chromosome, in this case, induced by radiation. When a break is induced in a chromosome in mature sperm, it remains in this condition until after the sperm has entered an egg. Following fusion, nuclear divisions begin, and a break in a chromosome can have drastic effects on the viability of the embryo as development proceeds. During early prophase
Prophase
Prophase, from the ancient Greek πρό and φάσις , is a stage of mitosis in which the chromatin condenses into a highly ordered structure called a chromosome in which the chromatin becomes visible. This process, called chromatin condensation, is mediated by the condensin complex...
the broken chromosome undergoes normal replication, but during metaphase
Metaphase
Metaphase, from the ancient Greek μετά and φάσις , is a stage of mitosis in the eukaryotic cell cycle in which condensed & highly coiled chromosomes, carrying genetic information, align in the middle of the cell before being separated into each of the two daughter cells...
the broken ends can fuse leading to the formation of a dicentric chromosome and an acentric fragment. The acentric fragment is frequently lost, while the dicentric fragment forms a bridge at anaphase
Anaphase
Anaphase, from the ancient Greek ἀνά and φάσις , is the stage of mitosis or meiosis when chromosomes move to opposite poles of the cell....
leading to another chromosomal break. This whole process then repeats itself, leading to the accumulation of serious imbalances in the genetic information of the daughter cells. The accumulation of this genetic damage finally leads to the death of the zygote (Fig. 1).
Diptera, Hymenoptera, and Coleoptera orders can be classed as radiation-sensitive, while Lepidoptera, Homoptera and mites (Acari) orders are radiation-resistant. A major difference between these two groups of Insects is that the former group has a localized centromere
Centromere
A centromere is a region of DNA typically found near the middle of a chromosome where two identical sister chromatids come closest in contact. It is involved in cell division as the point of mitotic spindle attachment...
(monokinetic), while the latter has a diffuse centromere (holokinetic),,,. However, more recent work suggested that lepidopteran chromosomes are intermediate between holokinetic and monocentric chromosomes. In any case, the centromere difference is believed to play a major, although not exclusive, role in radiation sensitivity. It was suggested, that possible molecular mechanisms responsible for the high radioresistance in Lepidoptera might include an inducible cell recovery system and a DNA repair probes.
Lepidoptera also do not show the classical breakage-fusion-bridge cycle that is a characteristic of dominant lethals induced in Diptera (Fig. 1). It appears that lepidopteran chromosomes can tolerate telomere loss without the drastic effects that this has on chromosomes in other orders. Lepidopteran chromosomes possess a localized kinetochore
Kinetochore
The kinetochore is the protein structure on chromatids where the spindle fibers attach during cell division to pull sister chromatids apart....
plate to which the spindle microtubules attach during cell division. The kinetochore plates are large and cover a significant portion of the chromosome length, ensuring that more radiation-induced breaks will not lead to the loss of chromosome fragments as is typical in species with monocentric chromosomes. In species with large kinetochore plates, the fragments may persist for a number of mitotic cell divisions, and can even be transmitted through germ cells to the next generation. The plates also reduce the risk of lethality caused by the formation of dicentric chromosomes, acentric fragments, and other unstable aberrations.
Field Application of Inherited sterility
The F1 sterile progeny produced in the field enhance the efficacy of released partially sterile males, and improve compatibility with other pest control strategies. For example, the presence of F1 sterile progeny can be used to increase the build-up of natural enemies in the field. In addition, F1 sterile progeny can be used to study the potential host and geographical ranges of exotic lepidopteran pests.Field programmes releasing irradiated moths under an SIT or inherited sterility approach have been in operation since the 1960s. The pink bollworm, Pectinophora gossypiella has been successfully contained since 1969 in cotton areas of the San Joaquin Valley in California and is being successfully targeted for eradication from cotton areas in the south-western USA and north-western Mexico. Since the early 1990s, the codling moth has been successfully suppressed in apple and pear production areas in the Okanagan Valley in British Columbia, Canada, and countries such as Argentina, Brazil and South Africa have plans or programmes against this pest. New Zealand eradicated outbreaks of the Australian painted apple moth, Teia anartoides. Mexico eradicated outbreaks of the cactus moth, Cactoblastis cactorum and the USA contains its advance along the Gulf of Mexico coast. South Africa has a programme to suppress the false codling moth, Thaumatotibia leucotreta in citrus orchards
Control of most moth pests is hampered by the increased resistance to the most widely used broad spectrum insecticides; hence the potential for expanded implementation of inherited sterility as part of an area-wide integrated approach is considerable.