**10. Conclusions**

#### **10.1. Are insect species undergoing domestication processes?**

Although few stunning cases (e.g., *B. mori*) have been the focus of abundant research, scientific literature has poorly investigated insect domestication to date. The main reason of this is that insect domestication for human food supply has been largely absent from the agricultural development with few exceptions [19, 73]. Moreover, it is likely that insect domestication study has been hindered by the complexity and the subjectivity of the definition of domesticated species (e.g., for *A. mellifera* [10, 16, 47, 117–119, 58, 89, 102, 110, 114–116]). The difficulty of defining a threshold along a continuous process is a common problem in biology (see similar debate about the status and the process for the species status *versus* speciation in [231–233]). Consequently, the study of the process is often set aside or eluded due to debates on a particular threshold. In insects, many scientific articles or books (e.g., [234]) have analyzed or reviewed the breeding/productions of various insect species without explicitly describing these processes as domestication. Yet, the human control on the life cycle (i.e., on individuals' life cycle in noneusocial species or on superorganism's life cycle in honey bees) of most produced insect species is congruent with a domestication process (**Figure 1**; *sensu* [12]). Since a large number of insect populations are produced in captive conditions isolated from their wild counterparts (**Figure 1**), many species can be considered as undergoing a domestication process. Moreover, new domestication processes can be expected in the near future due to current challenges to increase human food/sanitary security (e.g., [19, 164, 175, 186–188]) or to address new demands for pets (i.e., similar development to the ornamental fish trade (e.g., [18, 235–237])).

#### **10.2. Domestication patterns in insects**

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 (*Gromphadorhina portentosa*), mass/small-scale, and/or amateur production are practiced [198–202]. As for other "exotic" pets (e.g., [18]), these productions involve (i) a full control by humans on the life cycle in captive conditions since a large part of the production is completed out of the species native range and (ii), thus, an advanced domestication process (level 4, **Figure 1**).

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 (*Drosophila* spp.) [205–207].

*Drosophila* species first entered laboratories about 1900 and are now standard laboratory animals [208, 209]. As they become an instrument for scientific production, *Drosophila* have been massively produced in laboratory conditions in which life cycle, feeding, and mating are highly controlled by humans [208, 210–212]. This human control along with the strain development and artificial selection for particular purposes [208, 213–216] reflect an advanced domestication process of some populations (level 5, **Figure 1**), while there are many wild

Conversely to most other insect species, domestication of *Drosophila* populations has been the focus of several studies since it has been considered as a model system to understand the consequences of the domestication process on genomes and phenotypes [219]. Indeed, fruit flies are easy and cheaply to bred and have a rapid generation time (i.e., at least a dozen generations per year) [206, 220]. This allows comparing several populations that have or not been subject to different domestication histories (e.g., [221–223]) or even monitoring evolutionary trajectories of population undergoing a domestication process since their foundation from the wild [219, 224–226]. This has allowed studying domestication process in well-defined laboratory experiments with replication and specific environmental controls for several *Drosophila* species. An overview of these experiments allows highlighting the domestication consequences for *Drosophila* taxa. Different studies highlight that "domesticated" populations display genetic specificity and accumulation of deleterious mutations, inbreeding depression as well as increasing of fertility, tameness, and manageability due to selection for humanaccommodating phenotypes and/or the relaxation of selection on traits adapted in nature [219, 220, 222, 227–230]. Moreover, the evolutionary convergence is observed between long-

Although few stunning cases (e.g., *B. mori*) have been the focus of abundant research, scientific literature has poorly investigated insect domestication to date. The main reason of this

**9. Insects for laboratory research**

48 Animal Domestication

populations (e.g., [206, 217, 218]).

**10. Conclusions**

established laboratory populations [219, 220, 222, 227–230].

**10.1. Are insect species undergoing domestication processes?**

Domestication events in insects are no less complex than in crops and vertebrates. Domestication histories can involve (i) one (e.g., silkworms [61]) or several (e.g., in honey bees and bumble bees [113, 139]) domestication events and (ii) one (e.g., bumble bees [139]) 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 *B. terrestris*). Gene flow between populations at different domestication degrees is commonly observed in insects [59, 65, 119] but they do not hinder development of domestication syndrome (see next section).

Some insect species undergo domestication processes for several centuries (e.g., *B. mori* and *A. mellifera*; [57, 59, 60, 63, 89, 104, 105]), while domestications of most insects produced as biological control agents, pets, and laboratory organisms, or for SIT strategies and entomoceuticals' production have been recently initiated. These recent domestications have been made possible thanks to the advances in technology of captive environment control and animal food production since the nineteenth century [1]. Indeed, most insect domestications are thought to follow a directed pathway, which requires rapidly a full control of life cycle by humans in man-controlled environments. This implies the use of efficient environment and food control technologies. Technological advances have made possible or easier the domestication of species, which could not be domesticated in the past, paving the way to a new wave of domestication (similarly to aquatic species [28]).

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 [51]; aquatic species, e.g., water beetles [168]), behavior (i.e., solitary insects, e.g., silkworm [51]; eusocial species, e.g., honey bees [89]), and development (i.e., Endopterygota, e.g., honey bees [89]; Exopterygota, e.g., house crickets [19]); 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 *Drosophila* flies (i.e., laboratory organism) [139, 199, 208, 209].

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 *B. mori* to fly could result from a relaxation of selection in the wild (i.e., silkworm are protected and fed in captive conditions by humans) and/or a human pressure for "nonflying" insects (i.e., this facilitates the handling by humans). Similarly, the lower aggressiveness of honey bees can result from a lower predation pressure (i.e., human protection of hives) as well as from human selection for less aggressive populations. Inadvertent human habituation and unintentional conditioning could also be a primary selective agent in insect domestication as suggested

Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 51

to explain developmental and reproductive differences between *Drosophila* strains [220].

**10.4. Future prospects**

domestication process.

**Conflict of interest**

**Author details**

Thomas Lecocq

The author declares no conflict of interest.

Address all correspondence to: thomas.lecocq@univ-lorraine.fr

Université de Lorraine, Inra, URAFPA, Nancy, France

From a genetic point of view, animals in captive environment are expected to rapidly display genetic changes corresponding to adaptations to captive breeding [239]. Indeed, the specific selective pressure occurring in domestication environments promotes selection for domestication syndrome gene variants [11]. 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 [67] and melanin synthesis [68] of *B. mori*). Similarly, behavior modifications commonly observed in insect domestication syndrome (e.g., tameness, aggressiveness, manageability by humans) can be explained by mutations on neurogenetic genes affecting overall locomotion and activity as suggested in man-produced populations of *Drosophila* species and mammals [36, 220]. Therefore, large mutational target of neurogenetic genes can explain the evolution of specific behavior in animal populations undergoing domestication processes [220]. These neurogenomic loci collectively provide a large genomic substrate for variation to accumulate, and then selection and drift to act, to transform behavior [220].

The study of domestication of insect is still at a nascent stage. Some "model species" such as *A. mellifera*, *B. mori*, and *Drosophila* spp. have been the focus of several studies to understand domestication process. However, genetic bases of domestication-fostered modifications as well as the characterization of these modifications are poorly known. Therefore, further studies are needed to generalize domestication patterns as well as to understand genomic basis of

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 [19], raw materials [234], pets [194]). 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, *A. mellifera* that produces honey (i.e., the primary use) and edible pupae can be considered as the insect equivalent of dairy cows, which are valued not only for their milk but also as meat [19]. Moreover, honey bees provide several raw materials (wax), health food (royal jelly), entomoceuticals (venom), ecosystem service (pollination), model specimens for research [204], and pleasure (recreational beekeeping) to humans [92].

#### **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 [36]. 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 [36]. Some of these changes can be observed when comparing *B. mori* and its phylogenetically nearest wild counterpart [67–71] in tameness (i.e., larger tolerance to human presence/handling), aggressiveness (i.e., toward conspecifics since *B. mori* has higher ability to live in crowded conditions), morphology (i.e., leucism, larger body size), and reproduction/development (i.e., bigger cocoon and higher silk production, higher growth rate, altered premating behavior) [51, 52, 57, 68]. Comparison of silkworm specificities with phenotypes of man-produced *Drosophila* flies and honey bees shows some convergences: higher tameness (i.e., fruit flies), lower aggressiveness toward humans and conspecifics (i.e., in *A. mellifera*), modified reproduction (e.g., higher fertility in fruit flies; changes in reproduction, e.g., limited swarming in *A. mellifera*), and morphology (i.e., specific color patterns of man-controlled strains/races) [111, 121, 219, 220, 222, 227–230]. These specificities concern domestication traits facilitating the domestication by humans (e.g., aggressiveness in honey bees) as well as improvement traits (e.g., higher honey production in *A. mellifera*; higher silk production in *B. mori*) that increase the manageability and the animal production efficiency/profitability for humans.

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 *B. mori* to fly could result from a relaxation of selection in the wild (i.e., silkworm are protected and fed in captive conditions by humans) and/or a human pressure for "nonflying" insects (i.e., this facilitates the handling by humans). Similarly, the lower aggressiveness of honey bees can result from a lower predation pressure (i.e., human protection of hives) as well as from human selection for less aggressive populations. Inadvertent human habituation and unintentional conditioning could also be a primary selective agent in insect domestication as suggested to explain developmental and reproductive differences between *Drosophila* strains [220].

From a genetic point of view, animals in captive environment are expected to rapidly display genetic changes corresponding to adaptations to captive breeding [239]. Indeed, the specific selective pressure occurring in domestication environments promotes selection for domestication syndrome gene variants [11]. 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 [67] and melanin synthesis [68] of *B. mori*). Similarly, behavior modifications commonly observed in insect domestication syndrome (e.g., tameness, aggressiveness, manageability by humans) can be explained by mutations on neurogenetic genes affecting overall locomotion and activity as suggested in man-produced populations of *Drosophila* species and mammals [36, 220]. Therefore, large mutational target of neurogenetic genes can explain the evolution of specific behavior in animal populations undergoing domestication processes [220]. These neurogenomic loci collectively provide a large genomic substrate for variation to accumulate, and then selection and drift to act, to transform behavior [220].

#### **10.4. Future prospects**

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 [51]; aquatic species, e.g., water beetles [168]), behavior (i.e., solitary insects, e.g., silkworm [51]; eusocial species, e.g., honey bees [89]), and development (i.e., Endopterygota, e.g., honey bees [89]; Exopterygota, e.g., house crickets [19]); 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 cock-

roach (i.e., pet), or *Drosophila* flies (i.e., laboratory organism) [139, 199, 208, 209].

**10.3. Domestication consequences and their shaping factors**

50 Animal Domestication

manageability and the animal production efficiency/profitability for humans.

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 [19], raw materials [234], pets [194]). 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, *A. mellifera* that produces honey (i.e., the primary use) and edible pupae can be considered as the insect equivalent of dairy cows, which are valued not only for their milk but also as meat [19]. Moreover, honey bees provide several raw materials (wax), health food (royal jelly), entomoceuticals (venom), ecosystem service (pollination), model specimens for research [204], and pleasure (recreational beekeeping) to humans [92].

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 [36]. 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 [36]. Some of these changes can be observed when comparing *B. mori* and its phylogenetically nearest wild counterpart [67–71] in tameness (i.e., larger tolerance to human presence/handling), aggressiveness (i.e., toward conspecifics since *B. mori* has higher ability to live in crowded conditions), morphology (i.e., leucism, larger body size), and reproduction/development (i.e., bigger cocoon and higher silk production, higher growth rate, altered premating behavior) [51, 52, 57, 68]. Comparison of silkworm specificities with phenotypes of man-produced *Drosophila* flies and honey bees shows some convergences: higher tameness (i.e., fruit flies), lower aggressiveness toward humans and conspecifics (i.e., in *A. mellifera*), modified reproduction (e.g., higher fertility in fruit flies; changes in reproduction, e.g., limited swarming in *A. mellifera*), and morphology (i.e., specific color patterns of man-controlled strains/races) [111, 121, 219, 220, 222, 227–230]. These specificities concern domestication traits facilitating the domestication by humans (e.g., aggressiveness in honey bees) as well as improvement traits (e.g., higher honey production in *A. mellifera*; higher silk production in *B. mori*) that increase the

The study of domestication of insect is still at a nascent stage. Some "model species" such as *A. mellifera*, *B. mori*, and *Drosophila* spp. have been the focus of several studies to understand domestication process. However, genetic bases of domestication-fostered modifications as well as the characterization of these modifications are poorly known. Therefore, further studies are needed to generalize domestication patterns as well as to understand genomic basis of domestication process.

## **Conflict of interest**

The author declares no conflict of interest.
