Domestication has irrevocably impacted human evolution. The domestication process/pathways have been the focus of abundant research for plants and vertebrates. Advances in genetics and archeology have allowed tremendous progresses in the understanding of domestication for these organisms. In contrast, insects’ domestication has comparatively received far less attention to date. Yet, insects are the most common animal group on Earth and provide many valuable ecosystem services to humans. Therefore, the aims of this chapter are (i) to provide an overview of main ancient and recent insect domestication histories and (ii) to reread them by the light of the domestication process, pathways, triggers, and consequences observed in other animal species. Some of the considered species (i.e., silkworm and honey bee) have been chosen because they are among the few insects commonly acknowledged as domesticated, while others allow illustrating alternative domestication patterns. The overview of current literature shows similar human-directed pathway and domestication syndrome (e.g., increased tameness, decreased aggressiveness, modified reproduction) between several insect species.
- domestication level
- domestication pathways
- domestication syndrome
- insect species
Domestication is one of the most important developments in human history . Beginning during the Late Pleistocene with dog domestication [2, 3], it has irrevocably impacted human history, demography, and evolution leading to our current civilizations [1, 4, 5, 6]. Domesticated species play important roles for humans in many aspects of our daily life by providing food, biological control agents, pets, sporting animals, basic materials, and laboratory models [1, 7, 8]. This considerable importance in our culture, survival, and way of life has always aroused the curiosity of scientists and nonscientists. An extraction from the database Scopus of articles and reviews published since 1960 in Life Science Area (i.e., agricultural and biological sciences; biochemistry, genetics and molecular biology; environmental science; multidisciplinary) for which the term “domestication” is cited in the title, the abstract, or the keywords inventories 6199 documents (database accessed on August 31, 2018). However, despite this profusion of literature, significant questions regarding the domestication process, the domesticated species notion, or the domestication histories still remain [9, 10, 11].
The notions of domesticated species and domestication process are among the most confusing and controversial concepts in biology [12, 13, 14]. Vivid debates are continually fuelled by clashes of conflicting, although complementary, visions of botanists, mammalogists, ornithologists, ichthyologists, archeologists, geneticists, and sociologists. The achievement of a consensual view is impeded by the complexity of the domestication phenomenon, which involves many phylogenetically distant species and occurs in several different social and cultural contexts . Nevertheless, there were some attempts to unify the alternative points of view to some extent [1, 12, 13, 15, 16, 17]. For the purpose of this chapter, domestication can, thereby, be considered as the process in which populations are bred in man-controlled environment and modified across succeeding generations from their wild ancestors in ways making them more useful to humans who control, increasingly during the process, their reproduction and food supply [1, 12, 15, 16, 17]. This process does not involve all populations of a particular species: some populations can undergo domestication, while other populations do not. The domestication process is a continuum that can be divided into five key steps (the so-called “domestication levels”) based on the degree of human control over the population life cycle and the degree of gene flow from wild counterparts . This classification had been primarily developed for fish species [12, 18] but can be extended to other species (Figure 1). At the early stage (level 1) of the domestication process, the first attempts of acclimatization of a wild population to man-controlled environments are made . These environments can be captive or “ranch” conditions quite isolated from wild populations where living conditions, diet, and food are controlled by humans . The next stages correspond to an increasing control of the life cycle by humans: level 2—a part of life cycle is controlled by humans in man-controlled environments, but “seed” materials are collected in the wild to maintain rearing of the species (i.e., capture-based production; e.g., ); level 3—the life cycle is fully controlled by humans in man-controlled environments, but significant gene flow from the wild still occurs due to spontaneous introgressions or intentional wild specimen introductions by breeders ; level 4—the life cycle is fully controlled by humans in man-controlled environments without wild inputs . The last stage (level 5) corresponds to the development of selective breeding programs or organism engineering to intentionally modify some traits of the human-controlled populations (e.g., [22, 23, 24]). Seen from this perspective, a species can be considered as domesticated when it reaches, along this continuum, a threshold arbitrarily defined according to a particular scientific or legislative context. The resulting subjective definition of domesticated species is thus eluded from this chapter.
The domestication process is set during a temporal succession of interactions between a species and humans: the so-called “domestication pathways” [10, 25]. An overview of published domestication histories allows identifying three main pathways [10, 15, 25, 26]. In the commensal pathway, there is no intentional action on the part of humans but, as people manipulated their immediate surroundings, some populations of wild species have been attracted to elements of the human niche. The tamer, less aggressive individuals with shorter fight or flight distances of a wild species establish a profitable commensal relationship with humans. Later, succeeding generations of such individuals shift from cynanthropy to domestication through captivity setting up and human-controlled breeding. The dog and the cat are the archetypal commensal pathway species . Contrary to the former, the prey pathway begins with human actions, but the primary human motive is not to domesticate but to increase food resources. Actually, it is initiated when humans modify their hunting strategies into game-management strategies to increase prey availability, perhaps as a response to localized pressure on the supply of prey. Over time and with the more responsive populations (e.g., the more docile individuals), these game-management/keeping strategies turn into herd-management strategies based on a sustained multigenerational control over movements, feeding, and reproduction of populations corresponding to a domestication process. Species that have followed this prey pathway are, for instance, large terrestrial herbivorous mammals . At last, the directed pathway is the only one that begins with a deliberate and directed process initiated by humans in order to domesticate populations of a wild species . Most modern domestic species such as pets , transport animals , and aquatic species [12, 28] have arisen because of this pathway . The three pathways are theoretical conceptualizations of domestication process, but many species have a more complex history involving several pathways (e.g., pigs [10, 25, 29]).
When the domestication process begins, it results in long-term genetic differentiation and, finally, in the evolution of distinct changes in phenotypic traits [16, 30]. The differentiation of populations undergoing a domestication process can be initiated early in their domestication history and despite persistent gene flow from wild populations [21, 31, 32, 33, 34]. The resulting specific morphology, physiology, and behavior constitute the “domestication syndrome” that tends to be more of less similar among different species of a particular organism group [35, 36, 37, 38, 39, 40]. Overall, these specificities include domestication traits (i.e., facilitating the early stage of domestication) and improvement traits (i.e., appearing at latter stages of domestication) . The first are shared by all domesticates and generally fixed during the first stages of domestication, while the latter are observed in some domesticated populations when higher human impacts on breeding happens . These changes are driven by (i) selection pressures created by both unintentional and deliberate human actions as well as by human-modified environments and/or by (ii) a relaxation of the selection occurring in the wild [10, 41, 42].
The domestication process, pathways, and consequences on plants (e.g., [1, 37, 43]), mammals (e.g., [1, 10, 26]), birds (e.g., [44, 45]), and fishes (e.g., [12, 28]) have been the focus of an abundant research from Darwin’s works . However, insects’ domestication has comparatively received far less attention to date . Yet, insects are the most common animal group on Earth: they make up about 75% of all animal species [48, 49]. They play an important role in pollination, waste bioconversion, biocontrol, raw material supplying, food production, medical application, and human cultures. Strangely, major reviews on domestication give the impression that so few have been domesticated [10, 11, 15, 25, 26]. An overview of current literature shows how insect domestication has been overlooked: the database Scopus inventories only 68 papers that focus on it and most of them on only two species (i.e., the silkworm and the honey bee). Actually, most insect rearing/breeding/farming histories have not been considered as domestication processes although they can be interpreted as such. Therefore, the aims of this chapter are (i) to provide an overview of main ancient and recent insect domestication histories and (ii) to reread them by the light of the domestication process, pathways, triggers, and consequences observed in other animal species. Some of the considered species (silkworm and honey bee) have been chosen because they are among the few insects commonly acknowledged as domesticated species, while others have been considered since they allow illustrating alternative domestication patterns.
2. The silkworm and the sericulture
Silkworm is the caterpillar of the moth
Bombyx morilife cycle and production
The silkworm life cycle is strongly controlled by humans in indoor facilities with controlled environmental conditions . New eggs are incubated in rearing facilities where their hatching can be scheduled and synchronized by humans through chemical treatments and photothermal controls (e.g., black boxing practices) . The newly hatched caterpillars are transferred to rearing tray (i.e., brushing process) and fed by humans with man-produced plants (e.g., mulberry leaves) . After several molts, caterpillars climb on man-provided supports and spin their silken cocoons. Then, cocoons are collected and
2.2. Domestication history and pathway of
Even though silk spread rapidly across Eurasia, its production remained exclusively Chinese for several millennia [62, 66]. Indeed, the sericulture (i.e., the raising silkworms for silk production) spread only to Korea and Japan around 2000 years ago [57, 60] and was even later introduced to Central Asia and Europe (i.e., the Byzantines acquired the sericulture methods by 522 CE) through the Silk Road [57, 66]. This silkworm production expansion is one of the most tremendous examples of the direct and indirect consequences of the animal domestication on the human history . Indeed, the opening of Silk Road has dramatically impacted human history by triggering cultural/technical/good exchanges as well as population movements and disease spread out (e.g., bubonic plague) between Eurasian civilizations while its closing forced the merchants to take to the sea to ply their trade triggering the Age of Discovery [51, 66]. The industrial revolution and the increasing demand in Europe led to a peak of the sericulture by the eighteenth and nineteenth centuries before declining due to silkworm disease breakouts and the raising of cotton industry .
2.3. Consequences and progress of the domestication process in
3. The honey bees: beekeeping or apiculture?
Honey bees are eusocial insect species distinguished by their production and storage of honey and their construction of colonial nests from wax . They belong to the same genus (Hymenoptera, Apidae,
Apis melliferalife cycle and production
Unlike most of other bee species, honey bees produce perennial colonies with large number of individuals that (i) belong to different castes (i.e., workers that are sterile females, drones that are males, and queen that is the reproductive female) and (ii) are not able to survive by themselves for extended periods . In the nest, there is a labor division between castes: (i) the workers harvest pollen and nectar on flowers to feed larvae, queen, and other workers as well as to store food as honey [89, 93] and protect the nest from predators and (ii) queen ensures the production of new queens, drones, and workers . The colony is considered as a superorganism since it is a collection of agents, which can act in concert to produce phenomena (e.g., colony exhibit homeostasis and emergent behavior) governed by the collective . When environmental conditions are favorable (i.e., abundance of food), new queens are produced while old queen with up to two-thirds of the workers leaves the nest in a swarm to find a new location to establish a new nest . In the old nest, new queens compete until only one remains and the survivor takes the nest control . Then, the new queen goes on one or more nuptial flights and mates with several drones . Once mating is done, the queen remains in the hive and lays eggs . The swarming behavior and the takeover of the old nest by the new queen can be interpreted as the reproduction of the superorganism.
Humans can control the life cycle of the superorganism by providing man-made hives for the colony to live and store food . This allows humans to easily collect honey and other products that hive produces rather than to scavenge these products in the wild. More advanced practices allow apiarists to control colony reproduction by restricting swarming behavior and controlling mating by artificial insemination [96, 97].
3.2. Domestication history, traits, and pathway of
Molecular dating suggests that
Humans began harvesting wax and honey from honey bee colonies at least 9000 years ago [104, 105]. They originally scavenged these products from wild nests [89, 104, 105]. However, the demand for honey outgrew its natural availability as human populations became larger and sedentary . This context presumably triggered the beekeeping development by providing hives to honey bees that make it easier to harvest their honey and wax by humans . At the beginnings of beekeeping, honey bees were not “bred” so much as “kept”: humans provided rudimentary containers (often destroyed during honey harvesting) and hoped that wild bee colonies would take up residence without later swarming . Over time, humans increased their control on bees by developing swarming control device (i.e., queen excluder ), reproduction control (e.g., artificial insemination ), mass breeding (e.g., ), selective breeding programs (e.g., [108, 109, 110]), and new strains (e.g., Buckfast strain  or Africanized honey bees ).
The honey bees’ domestication concerns only
Domestication history of honey bees has been investigated through molecular datasets that highlight several domestication events followed by introgression between subspecies [90, 113, 114]. Although the honey bee domestication history has been regarded as a directed pathway , the evolution from early beekeeping practices to modern apiculture practices can been seen as similar to the prey pathway in which game-keeping strategies turns into control over movements, feeding, and reproduction. However, it is likely than directed and prey pathways occurred during honey bee domestication history since several domestication events happened [90, 113, 114].
Many authors acknowledge (often without justification) the domesticated status of
4. The bumble bees and the stingless bees: the other bee domestications
About 90% of world’s plant species are pollinated by animals [130, 131, 132], and the main animal pollinators in most ecosystems are bees . Although other taxa like butterflies, flies, beetles, wasps, or vertebrates can be important pollinators in certain habitats or for particular plants [133, 134], none achieves the numerical dominance as flower visitors worldwide as bees [130, 131]. The pollination efficiency of bees has been used by humans to improve their crop yields. The western honey bees is the most commonly used species in managed pollination service [76, 135]. This species pollinates nearly half of the top 115 global food commodities and is capable of increasing the yields of 96% of animal-pollinated crops [117, 136]. However, the lack of sufficient stocks of honey bees to ensure pollination service [115, 137], the aggressiveness of Africanized honey bees (i.e., obtained by man-made hybridization between African and European subspecies of
4.1. The bumble bees
Bumble bees (Hymenoptera, Apidae,
Although domestication of bumble bees has been acknowledged by various authors (e.g., [139, 147]), comparison between breeders’ stocks and wild populations is still lacking to highlight potential domestication syndrome in
4.2. The stingless bees
Stingless bees (Hymenoptera, Apidae, Meliponini) are social bees with perennial colonies (i.e., nest can remain active for more than 50 years) occurring in most tropical or subtropical areas [75, 148]. They are known for their pollen/honey production and their pollination efficiency for several valuable crops (e.g., coffee, Avocado, Strawberry, Rambutan) [138, 148]. Meliponiculture dates back to the Maya civilization and is nowadays practiced in Australia and Central/South America [148, 149, 150]. Nevertheless, their domestication process has not progressed so far (Level 2, Figure 1) since most of the meliponiculture is mainly a capture production that consists in attracting stingless bee swarms and maintaining the colonies in artificial wooden hives [148, 150].
5. Cochineal insects
Scale insects (Hemiptera, Coccoidea) are the third large insect groups including species that are, sometimes, considered as domesticated [47, 58, 151]: cochineals, lac scales,
Cochineal is an important source of red for dyes, lake pigments, cosmetics, and food/pharmaceutical colorants [151, 153]. Indeed, the red dye is mainly composed of carmine, which is a pigment obtained from the scale insects belonging to
The species is used as a source of carmine in Mesoamerica and South America since the pre-Columbian times . The earliest known cochineal-dyed textiles dates back to the twelfth century, but first evidence of cochineal farming is estimated to the tenth century [155, 156, 157]. The center of domestication is thought to be in Mexico . Carmine became an important export good during the Spanish colonial period . Later, the species was introduced in other areas such as Australia, Canary Islands, South Africa, and South Asia . In the middle of the nineteenth century, the production of cochineal fell sharply due to the development of artificial red dyes. Consequently, the cochineal trade almost totally disappeared in the twentieth century. Since the 1970s, cochineal production was restarted due to the discovery of carcinogenic and hazardous properties of synthesized dyes .
Lac is an important commercial resin of several utilities (e.g., material construction, cosmetics, medicine). It is a resinous secretion of lac insect species from Asia and Central America [160, 161].
6. Farmed edible and medicinal insects
Humans have been eating insects for millennia [58, 163]. However, human entomophagy is a long-standing taboo in westernized societies [19, 58, 164]. This can explain why insect farming for human food supply has been largely absent from the main agricultural innovations and domestications with few exceptions such as honey bees, silkworms (i.e., pupae is a by-product of silk production), and scale insects [19, 73]. Yet, more than 2 billion of people eat insect regularly since there are a source of protein, fat, vitamins, and minerals frequently stored and sold in developing countries (review in [73, 164]). Across the world, more than 2000 insect species are considered as edible for human food or animal feed [19, 58, 164, 165]. Beside food, insects provide many natural products for drugs to treat human diseases [166, 167].
Overall, the most commonly consumed insects by humans or livestock/pets are beetles (Coleoptera) (31%), caterpillars (Lepidoptera) (18%), bees/wasps/ants (Hymenoptera) (14%) as well as crickets (Orthoptera) (13%) [19, 58, 73, 163, 164, 165]. Most of these insects, as well as those used as entomoceuticals, are harvested in the wild  but some of these species are farmed for sale and profit [19, 73]. Currently, commercially farmed insects include (i) the house cricket (
7. Biological control agents and sterile insect technique
Addressing the needs of the increasing human population will require a 60% increase in global food production by 2050 . Insects could aid in achieving this objective by providing food production [19, 164] as well as pollination service (see Section 4) and biological control of pests .
Biological control is a method of controlling pests such as arthropods, weeds, and plant diseases using predator (e.g., ladybugs to control aphids , herbivorous, or parasite species ). Parasitoids are among the most widely used biological control agents (e.g., [177, 178]). In these species, female deposits its egg inside or outside a host where emerged parasitoid larva continues to feed resulting in the host death [178, 179, 180]. This parasitic way of life is used by humans to target hosts that are pests. Whiteflies parasitoids (Hymenoptera, Aphelinidae, Encyrtidae, Eulophidae, Platygastridae, Pteromalidae, and Signiphoridae) are an example of insects used in greenhouses to control major crop pests (i.e., the whiteflies; Hemiptera: Aleyrodidae) [177, 180]. As many other parasitoids (e.g., fly
The sterile insect technique (SIT) is an alternative approach to control main pests (e.g., [183, 184, 185]) or disease vectors (e.g., [186, 187, 188]). This method implies to massively release sterile males (sterilized through the effects of irradiation on the reproductive cells) of an insect species into a target environment to compete with wild males for reproduction [183, 184, 185]. Ultimately, mass releases allow limiting offspring production of a particular pest and promoting its eradication (e.g., ). Mass-rearing production with a life cycle fully controlled by humans is needed to produce the large quantity of insect required by SIT .
The required full control of life cycle of pest insects for SIT or biological control agents means that an advanced domestication process is reached (up to 5 since some patented strains are available ). In the context of SIT, several studies have investigated the differences between wild and mass-produced males in order to ensure that released sterile males are able to compete with wild males (e.g., [183, 190]). These studies show that the domestication process has triggered several ecological and behavioral divergences between produced and wild populations as well as a decreased fitness of produced populations in the wild (e.g., [183, 190]).
8. Insects as pets
Archeological pieces of evidence show that insects have been used as pets for centuries . Nowadays, crickets, grasshoppers, beetles, cockroaches, silkworms, ants, honey bees, bumble bees, mantises, and stick/leaf insects are bred by humans as a pleasing activity or for teaching purpose [192, 193, 194]. Conversely to vertebrates [8, 195, 196, 197], there is no, to my knowledge, scientific literature addressing the domestication of pet insects. However, some of these pet insects are produced for other purpose such as honey bees, silkworms, and house crickets for which a domestication process is acknowledged (see previous sections). For other species, such as hissing cockroach (
9. Insects for laboratory research
Animals are widely used as model species in biology and biomedical sciences. Some insect species have been used for laboratory experiments for several decades (e.g., silkworms, honey bees, and other species [54, 203, 204]), especially the fruit flies (
Conversely to most other insect species, domestication of
10.1. Are insect species undergoing domestication processes?
Although few stunning cases (e.g.,
10.2. Domestication patterns in insects
Domestication events in insects are no less complex than in crops and vertebrates. Domestication histories can involve (i) one (e.g., silkworms ) or several (e.g., in honey bees and bumble bees [113, 139]) domestication events and (ii) one (e.g., bumble bees ) or potentially several domestication pathways (e.g., honey bees). In most insect species (i.e., except for few extreme cases such as silkworms), different populations of a particular taxon can reach different degrees of progress in the domestication process (e.g., from wild status to an advanced domestication level in
Some insect species undergo domestication processes for several centuries (e.g.,
As for vertebrate species (see review in [1, 12]), some intrinsic features can hinder the development of domestication processes: (i) a diet that cannot be easily supplied by humans (e.g., oligolectic bee species feeding only on few plant species), (ii) long life-cycle (e.g., periodical cicadas that spend most of their 13- and 17-year lives underground at larval stage), (iii) bad disposition (e.g., some wasp species), or (iv) reluctance to breed in captivity. Nevertheless, modern technology could potentially allow domesticating any insect species. Indeed, current insect production involves species with very different ecologies (i.e., terrestrial taxa, e.g., silkworm ; aquatic species, e.g., water beetles ), behavior (i.e., solitary insects, e.g., silkworm ; eusocial species, e.g., honey bees ), and development (i.e., Endopterygota, e.g., honey bees ; Exopterygota, e.g., house crickets ); representative of the insect biodiversity. However, new domestication processes, which presumably occur only through directed or prey pathways for insects, are only initiated by humans to provide response to needs or demands of humanity. This means that the domestication of a species that could meet human needs/demands already addressed by another produced species is unlikely [1, 238]. Instead, all species that have recently undergone a domestication process and then have been massively produced are those which provide response to new needs or demands of humanity such as bumble bees (i.e., pollination in greenhouses), hissing cockroach (i.e., pet), or
An overview of current insect productions in man-controlled captive conditions shows that insect taxa are used to address very different human needs (e.g., food , raw materials , pets ). Moreover, many insect taxa that are primary produced to address a specific demand tend to be later used to serve several human needs as observed in the domestication histories of several mammal species. For instance,
10.3. Domestication consequences and their shaping factors
Overall, differentiations between wild populations and their counterparts undergoing a domestication process have been poorly studied in insect species. Yet, such divergences and convergences of various phenotypic traits that differentiate domesticates from their wild progenitors can be expected under the domestication syndrome hypothesis . In mammals, the domestication syndrome tends to comprise changes in tameness, aggressiveness, coat color/pigmentation, body morphology, reproductive alterations, hormone, neurotransmitter concentrations, and brain composition . Some of these changes can be observed when comparing
Specificities of populations undergoing a domestication process have been most likely shaped by unintentional/deliberate human actions, human-controlled environments, relaxation of the selection occurring in the wild or both as in other animal species [10, 41, 42]. For instance, the inability of
From a genetic point of view, animals in captive environment are expected to rapidly display genetic changes corresponding to adaptations to captive breeding . Indeed, the specific selective pressure occurring in domestication environments promotes selection for domestication syndrome gene variants . This selection on man-controlled populations can shape specific genotypes even when gene flow from the wild still occurs [21, 59]. Changes in traits linked to valuable resources for humans or morphology have been showed to have a genetic basis (e.g., specificity of silk gland transcriptomes  and melanin synthesis  of
10.4. Future prospects
The study of domestication of insect is still at a nascent stage. Some “model species” such as
Conflict of interest
The author declares no conflict of interest.