In female insects, reproduction generally involves producing yolky eggs, mating, and then laying fertilized eggs. Across the diversity of insects, however, different ways of reproducing illustrate an astounding variation in this simple series of events as well as divergence from it. In the most extreme examples, females can reproduce without supplying eggs with yolk, without mating, and even without laying eggs.
Female reproduction has been one of the most intensively studied aspects of insect biology in the past 50 years for two reasons. First, frequent confrontations between humans and insects in the arenas of agriculture and health make understanding insect reproduction of great practical importance. Production of the next generation of insects has several steps that are centered on the female. To reproduce, females need to make eggs or provide their embryos with nutrition in other ways. Once made, females must find an appropriate spot to deposit their eggs. For entomologists concerned with problem insects, these steps offer opportunities to disrupt reproduction and reduce the number of insects in the next generation. Second, the diversity of ways that insects reproduce provides a rich source of material for discovering the underlying rules of biology. For example, the extraordinary effectiveness of female insects in converting resources into eggs led to their use as an intensively studied model system. The process by which yolk is taken up into insect eggs serves as a model for how cells take up large molecules from the surrounding environment.
STRUCTURE OF FEMALE REPRODUCTIVE SYSTEMS
Female insects can make eggs, receive sperm, store sperm, manipulate sperm from different males, and lay eggs. Their reproductive systems are made up of a pair of ovaries, accessory glands, one or more spermathecae, and ducts connecting these parts. Ovaries make eggs, and accessory glands produce substances to help package and lay the eggs. Spermathecae store sperm for varying periods of time and, along with portions of the oviducts, can control sperm use. The ducts and spermathecae are lined with cuticle.
The ovaries are made up of a number of egg tubes, called ovarioles. The number of ovarioles varies with the type of insect, its size, and its particular life history. Clearly, the number of ovarioles and the number of eggs that can be produced by each set an upper limit to the total number of eggs, or young, an insect can produce. The rate that eggs can develop is also influenced by ovariole design. In meroistic ovaries, the eggs-to-be divide repeatedly and most of the daughter cells become helper cells for a single oocyte in the cluster. In panoistic ovaries, each egg-to-be produced by stem germ cells develops into an oocyte; there are no helper cells from the germ line. Production of eggs by panoistic ovaries tends to be slower than that by meroistic ovaries.
Accessory glands or glandular parts of the oviducts produce a variety of substances for sperm maintenance, transport, and fertilization, as well as for protection of eggs. They can produce glue and protective substances for coating eggs or tough coverings for a batch of eggs called oothecae.
Spermathecae are tubes or sacs in which sperm can be stored between the time of mating and the time an egg is fertilized. Paternity testing of insects has revealed that some, and probably many, female insects use the spermatheca and various ducts to control or bias sperm used in favor of some males over others.
COMMON AND DIVERSE MODES OF REPRODUCTION
The most common mode of reproduction in insects is by yolked eggs, fertilized internally, that are laid outside the body. However, other modes of reproduction are not uncommon. Insects with unusual and even unique modes of reproduction are interesting as examples of extreme biological forms and processes. Modes of reproduction vary in three important aspects: whether eggs are fertilized, whether eggs are provisioned, and where embryonic development takes place.
First, reproduction without fertilization, or parthenogenesis, is common in insects as a normal means of reproduction in addition to or instead of sexual reproduction. For example, the system of sex determination in the Hymenoptera relies on parthenogenetic production of males. Virtually the entire order produces males from unfertilized haploid eggs and female from fertilized diploid eggs. This type of sex determination, called haplodiploidy, is also found in some Sternorryncha, Thysanoptera, and Coleoptera.
In another common type of parthenogenesis, germ stem cells in the ovary do not go through meiosis before they start development. As a result, offspring are clones of the mothers, having a full copy of her genes. Aphids are the premier example of this type of parthenogenesis. In a third type, meiosis occurs but the diploid number of chromosomes is restored by fusion of two nuclei. This type of parthenogenesis has been particularly well studied in stick insects (Phasmida). A fourth type requires mating, but fertilization is not completed. Sperm is necessary for development to begin, but the male’s genes are discarded. Sperm-dependent parthenogenesis is found in some bark beetles.
A second important factor that defines the mode of development is the amount of yolk material provided to the egg. Amount of yolk can vary from none to more than enough to complete development. When eggs are laid without provisioning, nutrition must be obtained from elsewhere. Females of some insects, such as aphids, can keep developing embryos in their bodies and supply them directly with needed nutrients. In contrast, some parasitic and parasitoid wasps (e.g., Trigonalidae, Braconidae) and flies (Tachnidae) produce tiny eggs lacking yolk and lay them inside other insects that can provide for them.
A third important descriptor of developmental mode is the site of embryonic development. Most eggs are laid outside the mother’s body but, in ovoviparous insects, eggs can be retained inside the body of the mother where the embryos develop. At hatching, they are released to the outside world. In true viviparity, embryos also develop in the mother’s body but there is no intermediate egg stage. The site of development of parasitoids is similar to that in viviparous insects, in that it is inside another insect. Development of parasitoids, however, takes place in the bodies of host insects, rather than in the mother.
MANAGEMENT OF NUTRIENTS FOR EGGS
I n the common mode of reproduction by yolked eggs, female insects accumulate large amounts of macronutrients, especially protein and fat. Lipids are usually derived from carbohydrates in the diet and are not generally in short supply. Amino acids, particularly essential amino acids, can be limiting. Therefore these are a particularly important part of the yolk.
Eggs may be provisioned with nutrients obtained in either the larval or the adult stage or both. Insects that do not feed as adults and have their lifetime’s egg production completed when they become adults can draw only on larval nutrients. Even insects that feed after eclosion can use excess larval nutrients to provision eggs.
Mosquitoes and other blood-feeding Diptera provide examples of the often interlocking roles of larval and adult feeding. Female mosquitoes feed on nectar and vertebrate blood to obtain nutrients for egg production. In some mosquitoes, however, food eaten during the larval stage supports the production of at least some eggs. The ability to produce eggs without blood feeding is called autogeny. Some autogenous species can mature their eggs only this way and have lost the ability to feed on hosts. Other species are more flexible and can use leftover reserves, if they are available, but can feed on blood immediately if they are not. In addition, when species occur over a broad geographical area, they can be locally adapted. The pitcherplant mosquito, Wyeomyia smithii, is completely autogenous in the northeastern United States, where larval densities are low and food more abundant, but must feed on blood in the southeast, where larval resources are more scarce.
Aspects of both larval and adult environments can favor autog-eny. A larval environment that offers more consistent resources than the adult one will favor obligate autogeny, whereas more predictably abundant food in the adult environment will favor obligate blood feeding. In the Northern Hemisphere, autogeny becomes more common toward the arctic, where host vertebrates are less abundant. Short-term variability in nutritional resources, either in a patchy spatial environment or over time, can make physiological flexibility, termed facultative autogeny, a better strategy than obligate autogeny.
Males can be an important source of nutrients especially when the female’s resources are limited. Nutritional contributions are especially conspicuous in Orthoptera, which transfer large sper-matophores that can weigh over 20% of the male’s body weight. In a variety of insects, proteins transferred to females during mating have been found in their eggs, ovaries, blood, and various body parts.
TRANSFER OF SPERM AND POSTMATING MANAGEMENT
Fertilization of eggs is the focus of sexual selection. Natural selection biases survival toward individuals that are most successful in their environment. Sexual selection biases its rewards toward those individuals that enhance the success of their own genotype in the next generation through any aspect of mating and subsequent fertilization.
Classically, males compete with each other for access to females, and females can choose to mate with them or not. Because insects have internal fertilization, there are many possibilities for females to manipulate sperm after mating. When females mate multiple times, male competition can take place between sperm in the female reproductive tract. Overlooked for many years, it is now known that the female may also have control over which male’s sperm will fertilize her eggs. Mechanisms that females use to bias paternity include active elimination of sperm, digestion of sperm, lack of sperm transport to the spermatheca, and decreased use of some sperm batches in fertilization. Postmating female choice is often called cryptic female choice, although it is no more cryptic than postmating competition between sperm.
Females are generally believed to choose their mates based on features that indicate their quality as parents. For example, a choice can be made based on behaviors such as gifts of food or some other indicator of resources, on the amount of sperm transferred, or on the concentration of a protective chemical given to the female. In addition to features that indicate success under the rules of natural and sexual selection, females may also choose sperm or mates based on genotypes that are most complementary with their own.
Highly social insects, especially those in perennial colonies, provide an interesting variation in female reproductive strategies. For example, to produce enough worker insects, queens must have a large supply of sperm. Only a small proportion of total sperm is used to produce new queens and males; most of it is used to make more workers. In social Hymenoptera, which includes ants, bees, and wasps, males can be produced without sperm because males develop from unfertilized eggs. As far as is known, new queens mate only before starting or joining a colony and must, therefore, at that time store as much sperm as they will need for the remainder of their lives. One important factor that affects colony longevity is the amount of sperm available for fertilizing eggs. Queens of large leaf-cutting ants (Atta) mate many times and store as many as 250 million sperm. In contrast, termites do not have to store large amounts of sperm because termite colonies are headed by both a queen and a king, and mating takes place throughout their lives.
Ants, the most speciose of the social insects, have a wide range of colony sizes and rates of worker production. Across the group, the number of sperm stored is correlated with the number of ovarioles, which suggests that there is a cost to long-term sperm storage and that sperm storage is matched to the lifetime needs of a successful colony queen.
The culmination of insect reproduction is typically the oviposition of mature, fertilized eggs in an environment that will support their development. Eggs can be placed on surfaces, in crevices, in soil, and in animal or plant tissue, and accessory glands produce secretions used to protect eggs. Females often have a structure called an ovipositor, which is made up of modified appendages on the last abdominal segments and serves as a tool for penetrating substrates. For example, many grasshoppers use their ovipositors to dig into soil, where they lay eggs in a frothy matrix. Also, some parasitic wasps have long, needle-like ovipositors that can drill through wood to reach host insects.
Oviposition can be linked physiologically to prior events in egg maturation. For example, insects that mature eggs throughout the adult stage can often adjust their egg production based on available oviposition sites as well as on available nutrition. When oviposition sites are rare, unlaid eggs can inhibit the hormonal control network that guides egg maturation. Delayed oviposition can go further than slowing egg production and lead to resorption of eggs, which reallocates resources away from reproduction and toward survival.
Oviposition sites also provide sensory cues that can stimulate further egg maturation. For example, egg production in newly eclosed females in the diamondback moth, Plutella xylostella, is accelerated by the presence of single volatile components of host cabbage plants. Ovarian response to oviposition and related cues can reduce the opportunity costs females suffer when the supply of completed eggs does not match the availability of oviposition sites.
Protection of eggs, particularly those laid in clusters, can be extended by parental care. For example, egg guarding reduces the risk of eggs being used by parasitoids or eaten by predators.