Parental Care (Insects)

Parental care in insects ranges from covering eggs with a protective coating to remaining to feed and protect young, to forming eusocial societies with alloparental care and lifelong associations of parents and offspring. Most commonly, care is provided solely by females; males rarely care for eggs and young alone, but in some cases males and females form long associations to rear young to adulthood (Table I). Parental care has evolved independently many times, and examples do not follow along phyloge-netic lines. Various forms are widespread taxonomically and care is most developed in Hemiptera (true bugs), Thysanoptera (thrips), Embiidina (webspinners), Coleoptera (beetles), Hymenoptera (ants, bees, and wasps), and Isoptera (termites).

aNumber of orders in which parents exhibit the behaviors listed. bKey: EP, either or both parents cover eggs before abandonment; EC, either or both parents remain and guard eggs; YC, either or both parents remain with young and care for them; YP, either or both parents provision young or regurgitate food to them; OV, females extend development internally and are ovoviviparous, larviparous, or viviparous; PZ, males provide prezygotic investment.

FORMS OF PARENTAL CARE

Maternal Care

The most rudimentary form of maternal care is provided by females that incorporate toxins into their eggs, oviposit them in protected places, or cover their eggs with a hard shell or wax-like compound before abandoning them (Table I). For example, embiopteran webspinner females, Antipalurai urichi, cover their eggs with layers of macerated bark and other substrate materials and silk to protect them from hymenopteran parasites. Webspinner maternal care is more complex and extensive than egg protection, and these females construct silk galleries and remain with their eggs and nymphs.
Many species of insects guard their young against predators by using chemicals or defensive behaviors. Care may end when young hatch, or it may extend until larvae or nymphs are mature. For example, eggplant lace bugs, Gargaphia solani, guard their eggs and gregarious nymphs until maturity; if a predator approaches, the female rushes at it, fanning her wings.
A second major function of maternal care is to facilitate feeding. A plant-feeding membracid bug, Umbonia crassicornis, cuts slits in the bark with her ovipositor to facilitate nymphal feeding. She remains with the nymphs, actively maintaining feeding aggregations until the young reach adulthood. Parental care often comprises a suite of adaptations of multiple behaviors that serve multiple functions. A well-cited example of a complex of behaviors is the female salt-marsh beetle, Bledius spectabalis, which maintains a burrow shaped in a way that prevents flooding during high tide. She also provisions the young with algae, prevents mold, and protects the vulnerable first instars from attack by parasitic wasps.
In some insects, maternal investment takes the form of a period of internal development. Among insects, cockroaches carry this investment to the extreme and show the entire range of reproductive modes and maternal care. The oviparous German cockroach, Blattella germanica, carries her egg sac externally until nymphs hatch, and Blattella vaga produces maternal secretions on which her neonates briefly feed. In ovoviviparous species, eggs develop inside the body of the mother and have sufficient yolk to complete development. The viviparous cockroach, Diploptera punctata, displays a remarkable form of parental care. Females undergo a 60-day “pregnancy” during which highly nutritious milk, secreted from the walls of the brood sac, is ingested orally by the developing young. At birth, young are in an advanced state of development, and care is terminated shortly after birth.

Paternal Care

Exclusive paternal care of eggs or young is restricted to about 100 species of insects, almost all within the Hemiptera. For example, in a giant water bug, Abedus herberti, females adhere their eggs to the wing covers of a male, who stops feeding and instead spends his time until eggs hatch aerating and protecting them from predators. Males of the subsocial spider-hunting wasp, Trypoxylon superbum. are an unusual example from the Hymenoptera. After females provision and seal the cells, males remain to guard nests against parasitism and ant predation.
Indirect paternal contributions to offspring are widespread in a number of taxa. Males may invest in offspring with nutritional offerings to the female in the form of nuptial gifts of captured prey items or even their own bodies. They may transfer proteins or protective substances in a spermatophore. Male katydids, for example, provide a spermatophore during copulation that may be as much as 40% of their body mass; spermatophore nutrients have been shown to be important to the reproductive success of females. Male arctiid moths, Utetheisa ornatrix. provide a different sort of indirect paternal contribution when they transfer protective pyrrolizidine alkaloids to females during mating. These alkaloids are passed to the eggs, which are then unappealing to predators.

Biparental Care

Biparental care of offspring is restricted to beetles, termites, and cockroaches, and may include earwigs. It can be very elaborate and extensive. For example, the woodroach, Cryptocercus punctulatus, and all termites form life-long family associations. Male and female construct and guard an extensive tunnel system or a nest, and they protect and facilitate feeding of young until the offspring reach maturity. Woodroaches care for a single brood for 3 or more years, feeding them on hindgut secretions containing symbiotic fauna necessary to digest their wood diet. In many of the “higher termites,” (e.g., Rhinotermitidae and the Termitidae), few or no workers or soldiers reproduce; rather, they remain as alloparents. Task specializations based on morphology and sex is strongly expressed. Primary reproductives may live 20 years or more, whereas workers and soldiers often live less than a year.
In another well-studied example, male and female burying beetles cooperate to bury and prepare small vertebrate carcasses to serve as the food source for their young. Both parents treat the carcass with preservative anal and oral secretions; both regurgitate semidigested protein to the begging larvae (Fig. 1). In the burying beetle, Nicrophorus orbicollis, males commonly remain in the nest until larvae are half-grown and the carcass is substantially consumed; females remain until larval development is complete and may even accompany larvae during the wandering stage. As with most species with biparental care, male and female burying beetles do not have exclusive, specialized tasks. When both parents are present, females feed larvae more often than males; but if the male becomes a single parent, he compensates for the loss of a mate with increased feeding

FIGURE 1 Female N. orbicollis regurgitates to larvae while the male, in the background, keeps the carcass free of fungi.
rates. However, in another species with biparental care, the dung beetle, Cephalodesmius armiger, there is some task specialization. Male and female form a permanent pair-bond to rear one brood in a subterranean nest. Males forage outside for plant material that females process into brood balls into which they lay a single egg. Males continue to forage, and females enlarge the brood ball as the larvae grow.

EVOLUTION OF PARENTAL CARE

Problems of resource exploitation are central to the evolution of parental care. The spatial and temporal distribution of food sources and their physical and ecological characteristics have shaped the convergent life-history characteristics and behavior of insects that provide care. The dispersion, quality, and persistence of resources influence how sedentary or nomadic a species is and what competitors, predators, and parasites it must deal with. These in turn, determine if parental care can be an effective strategy, that is, when there is something that parents are able to do to increase the survival of young. Parental care is often associated with territoriality and spatial fidelity. Thus, wood is a stable resource that provides both food and shelter but is difficult to exploit. Once a nest has been established, it can be defended; adults are often necessary to inoculate young with gut symbionts to digest wood or to otherwise prepare it for consumption. Dung and carrion feeders exploit a rich but unpredictable resource that can be buried to reduce competition. Foliovores may be somewhat more nomadic and are usually exposed to heavy preda-tion and parasitism. Parental defense of eggs or young can be effective and can considerably improve survival. Predators and detritivores often depend on patchy resources. Parents may collect and transport food to young that are sequestered in a sheltered nest or burrow.
Parental care is also favored by limited lifetime reproductive opportunities. Valuable but unpredictable resources (carrion or dung) or resources that are hard to acquire (a tunnel system) are especially potent selective forces for parental care. Both involve the construction of elaborate nests that represent a substantial investment. These resources are associated with the production of fewer and smaller clutches of larger young. Burying beetles, dung beetles, and woodroaches produce on average only a single brood in a lifetime. Biparental care is associated with these species both because male assistance in guarding and provisioning can often greatly increase the survival of the young and because there are few additional mating/breeding opportunities. The improved survival of his young offsets the male parent’s potential gain if he were to leave and search for rare carrion or females when most individuals in the population are mated.
Exclusive paternal care is rare in insects because external fertilization is rare. Internal fertilization both reduces the certainty of paternity if females have multiple mates and disassociates the father from his offspring when they appear. These factors discourage paternal care and encourage maternal care in other taxa. Exclusive paternal care is associated with fidelity to a nest site, including a “nest” of his own wing covers, and with the ability of the male to guard the clutch of multiple females. Under these conditions, a male does not forgo additional matings; in fact, the demonstration of paternal behavior may increase his attractiveness to females.
No single factor or suite of factors can predict the evolution of care. Parental behaviors serve multiple functions, and seemingly the same environments and resources harbor parental and nonparen-tal members of a family. In addition, the evolution of parental care involves a suite of secondary changes, including greater dependence on the part of the young and the loss of adaptations for independence from parents. Burying beetle larvae, for example, have no defenses and are initially dependent on parental regurgitations unlike their carrion beetle relatives that are fully armored and independent.
Thus, insects not only show a variety of forms of parental care, but also many demonstrate behavioral plasticity that allows them to adjust the level or form of care to changing circumstances, such as the loss of a mate. As more examples come to light and familiar ones are better studied, it becomes clear that the functions of care are also varied and complex even within a single species. This variety is not surprising, since parental care has evolved independently many times in insects in response to different selective forces.