**2. Genomic insight in pig domestication**

their wild progenitors. The meaning of the word domestication is poorly defined and lacks consistency across different scientific disciplines [1]. From a population genetics perspective, domestication results in a deliberate separation of the captive, and then domesticated population from its parent population. Domestication is, therefore, initially indistinguishable from any other event that results in reduction of gene-flow between populations, and creating opportunity to respond to new selective pressures [2]. The simplest definition of domestication considers a domestic population as a subset of the wild population with cessation of gene-flow [3]. Therefore, one can expect that domestication results in a reduction of genetic variation in the domesticated population. The onset of domestication occurred in multiple geographically distinct areas during the late Pleistocene to early Holocene transition (12,000–8200 B.P, [4]). The process of land animal domestication, however, turns out to be a complex, long-term event initiated by cultural transitions related to food production [5, 6]. The definition of an animal to be considered domesticated varies, however, some common characteristics emerge from literature. Teletchea and Fontaine propose that a domesticated animal should be selectively bred in captivity and modified from its wild ancestors [7]. It is important to realize that those early considered domestic populations were genetically and phenotypically hardly distinguishable from wild types, and therefore geographical location was a better predictor of local characteristics than domestication status [3]. The general assumption that multiple centers of domestication exist has important implications for the source of genetic and phenotypic variation in domesticated species. In cattle, for example, two distinct cattle lineages that separated ~300,000 ya, contributed to two major lineages of extant cattle, that is, taurine cattle (originating from *Bos taurus*) and indicine cattle (originating from *Bos indicus*) [8]. It is not unlikely that multiple populations of wild land animals that are now extinct contributed to the genetic diversity that is observed in modern breeds [9]. The domestic animal populations accompanying human settlements did not necessarily remain at their original location of domestication. Rather, they moved along with early farmers spreading in Asia and from Eastern Anatolia throughout Europe [10]. During this process, the connection of domestic animals and farmers was relatively loose, enabling animals to hybridize with local wild populations [11]. Only centuries later, animals were actually kept in strict enclosures and intentionally bred for specific purposes, leading towards the best-known characteristic of domestic animals: docility [12]. This controlled environment drastically reduced the opportunity of domestic herds to interbreed with local wild populations, which enabled strong divergence between domestic and wild forms. We should realize the genetic basis of the modifications leading towards morphological differences in domestic animals compared to their wild ancestors is mostly provided by standing genetic variation, that is, mutations that were already present before the onset of domestication and selection. Therefore, indicating the genetic underpinnings of domestication remain challenging [13, 14]. Arguably, we can speak about a domestic population if not only the gene pool is distinct from the wild variety, but also (artificially) selected variants leading to desired phenotypes are at high(er) frequency in the domestic population [15–18]. In this chapter, an in-depth overview is provided for the complex process of domestication, admixture, and selection leading towards the genetic diversity in extant breeds, using pig

as model.

22 Animal Domestication

Domesticated species are good models to study genomic and phenotypic consequences of demography and selection [19]. The use of higher DNA marker densities has enabled researchers to reveal the complexity of livestock domestication, which was shown to be far more complex than a single sampling from the wild [20]. Genotyping and sequencing technologies have opened up many opportunities to reveal the complex history of domestication, admixture, and selection in livestock [4, 20]. Combining modern sequence technologies with extensive studies on fossil records and land animal usage now enables the reconstruction of domestication in details. Apart from a suitable history and documentation, the availability of detailed genetic information is crucial to be able to study genomic alterations due to domestication. Pig (*Sus scrofa*, Linnaeus, 1758) was the first livestock species for which a genome consortium was established with the intention to completely map the genome [21, 22]. The design of a 60k single nucleotide polymorphism (SNP) chip for pigs in 2009 greatly contributed to the applicability of genomics techniques in pig breeding, and simultaneously increased possibilities for population genomics studies [23]. The establishment of a consortium to sequence the pig genome in 2003 and publication of the pig reference genome in 2012 opened up an even greater window of opportunities to study various aspects of the genetics of pig, since the highest resolution possible became reality [21, 24]. Together with the evolutionary history of pig, these provide an unprecedented study system to demonstrate the impact of domestication from a genomics perspective. Pig genomes contain a complex composition of segments, reflecting the different backgrounds that contributed to the domestic animal it is today. Disentangling these genomic signatures provides enormous information about the complex background and history of the worlds' most consumed meat type [25].

#### **3. Conceptual history of the pig (***Sus scrofa***)**

Here I will discuss genomic variation within and between different populations of pigs, providing deeper understanding of how domestication has influenced genetic diversity of pigs. Five major events in the evolutionary history and domestication of pigs can be recognized that are of importance for the distribution of genetic variation in modern pig genomes (**Figure 1**).

#### **3.1. Speciation of** *Sus* **in island South-East Asia**

Knowledge about the source of the domesticated form, the origin of the species, is essential to understand genetic variation within modern breeds. The Suidae family is particularly interesting for molecular genetic studies as it is one of the few mammalian lineages that has closely related species living today. Multiple *Sus* species originated roughly ~4 million years ago on Island Southeast Asia (ISEA). The island structure in this region probably promoted speciation, since the bearded pig *Sus barbatus*, the warty pigs *S. celebensis* and *S. verrucosus* but also wild *S. scrofa* occur on separate islands. The phylogenetic structure within the genus *Sus*

wild boars, but the reduction was most severe in Europe [24]. The geographic distribution of wild boar over Europe faced another severe decline starting in the middle ages and lasted until the late eighteenth century [25]. In the mid-nineteenth century, natural or human-mediated recolonization events resulted in isolated populations expanding their range. Some of these isolated populations were small in effective size for decades or longer, causing inbreeding and population differentiation. Local re-stocking of populations with geographically distinct wild boar resulted in complex genetic structures and signatures of population dynamics [31, 32]. Such complex genetic architectures have been detected in Italian and Luxembourgian wild boars. However, these mixed genomes could have been shaped due to ancient glaciation events [33] or because of recent mixture [34]. Asian *Sus scrofa* is thought to have had a larger effective population size which, together with its proximity to the origin of the species, results in higher genetic diversity compared to the European clade [24, 35, 36]. These highly distinct groups of wild boar provided the basis of the genetic background of the later

A Genomics Perspective on Pig Domestication http://dx.doi.org/10.5772/intechopen.82646 25

The demographic and geographic history of the domesticated pig may be just as complex as that of its wild counterpart. There is compelling evidence that pig domestication events occurred at multiple locations, Eastern Anatolia and China independently, some 9000–10,000 years ago [26, 37]. Domestication has not been a single event, but rather a long period with recurrent admixture with wild populations [38]. Following initial domestication, the traits selected as well as how animals were kept, strongly differed in Europe and Asia resulting in highly different domesticated pigs between Europe and Asia. Asian pigs were kept in close proximity of humans, often integrated in their settlements. By contrast, European pigs were roaming freely in forested areas in the surroundings [39, 40]. Only during the Industrial Revolution, a more strict pig farming system was adopted and implemented to fulfill the increasing demand for pork. Because of recurrent gene-flow between wild and domestic pigs, a reduction in genetic diversity cannot be observed in domesticated pigs compared to their presumed wild counterparts [35, 38, 41]. One should realize though that European and Asian domesticated pigs have been geographically isolated for over a million years ago, because they have distinct wild origins. Therefore, they genetically resemble local wild boar more than domestic pigs from different geographic origins [24, 35]. This dichotomy also underlies the fact that European pigs

and wild boar are genetically less diverse than Asian wild boar and domestic pigs.

It is well documented that during the Industrial Revolution in Europe, European pigs have been deliberately hybridized with Asian pigs. Urbanization in Europe increased the demand for meat such as pork, but during those times, pig farmers would still have their pigs roaming in surrounding forests. Forest cover was decreasing and a different pig production system seemed inevitable [40]. Due to this changing environment, pig breeders sought a way to improve their stock in such way that pigs had to become adapted to living in small(er) enclosures, be more prolific and gain weight more rapidly. This led to selection for traits better adapted to

**3.4. Hybridization between domesticated pigs of different origin**

domesticated pigs.

**3.3. Independent domestication leading to separate clades**

**Figure 1.** Schematic overview of the history of the pig (*Sus scrofa*). Five main events in pig history are indicated in blue, with the approximate timing of those events in red: (1) Speciation of *Sus* species in Island South-East Asia (ISEA). (2) Divergence between European and Asian *S. scrofa* lineages. (3) Independent domestication leading to separate domesticated clades in Europe and Asia. (4) Hybridization between domesticated pigs from Asia and Europe. (5) Breed formation.

has been studied intensively and revealed a complex history of admixture [26, 27]. The past connection of landmasses at the Sunda shelf and isolation of Indonesian islands by the rapid sea level rise after the last glaciation period [28] created a dynamic process of (re)colonization, isolation and admixture of different *Sus* species and populations [29, 30]. The species that gave rise to the domesticated pig, *Sus scrofa*, has its origin in Southeast Asia some ~4 Mya and colonized almost the entire Eurasian mainland from there. The widespread and opportunistic nature of this species probably contributed to the fact that *Sus scrofa* is the only pig species that was successfully domesticated [25].

#### **3.2. Divergence between European and Asian** *S. scrofa*

*Sus scrofa* is widespread within Eurasia (**Figure 1**) and consists of many isolated wild and domesticated populations. The divergence between Western-European and Eastern-Asian populations has been estimated at about 1.2 Mya [24, 29], and has resulted in many fixed molecular differences between the two groups. This divergence not only resulted in a European and an Asian *S. scrofa* clade, but also in differences in demographic history and population size. The last glacial maximum probably reduced population sizes of both European and Asian wild boars, but the reduction was most severe in Europe [24]. The geographic distribution of wild boar over Europe faced another severe decline starting in the middle ages and lasted until the late eighteenth century [25]. In the mid-nineteenth century, natural or human-mediated recolonization events resulted in isolated populations expanding their range. Some of these isolated populations were small in effective size for decades or longer, causing inbreeding and population differentiation. Local re-stocking of populations with geographically distinct wild boar resulted in complex genetic structures and signatures of population dynamics [31, 32]. Such complex genetic architectures have been detected in Italian and Luxembourgian wild boars. However, these mixed genomes could have been shaped due to ancient glaciation events [33] or because of recent mixture [34]. Asian *Sus scrofa* is thought to have had a larger effective population size which, together with its proximity to the origin of the species, results in higher genetic diversity compared to the European clade [24, 35, 36]. These highly distinct groups of wild boar provided the basis of the genetic background of the later domesticated pigs.

#### **3.3. Independent domestication leading to separate clades**

has been studied intensively and revealed a complex history of admixture [26, 27]. The past connection of landmasses at the Sunda shelf and isolation of Indonesian islands by the rapid sea level rise after the last glaciation period [28] created a dynamic process of (re)colonization, isolation and admixture of different *Sus* species and populations [29, 30]. The species that gave rise to the domesticated pig, *Sus scrofa*, has its origin in Southeast Asia some ~4 Mya and colonized almost the entire Eurasian mainland from there. The widespread and opportunistic nature of this species probably contributed to the fact that *Sus scrofa* is the only pig species that

**Figure 1.** Schematic overview of the history of the pig (*Sus scrofa*). Five main events in pig history are indicated in blue, with the approximate timing of those events in red: (1) Speciation of *Sus* species in Island South-East Asia (ISEA). (2) Divergence between European and Asian *S. scrofa* lineages. (3) Independent domestication leading to separate domesticated clades in Europe and Asia. (4) Hybridization between domesticated pigs from Asia and Europe. (5) Breed

*Sus scrofa* is widespread within Eurasia (**Figure 1**) and consists of many isolated wild and domesticated populations. The divergence between Western-European and Eastern-Asian populations has been estimated at about 1.2 Mya [24, 29], and has resulted in many fixed molecular differences between the two groups. This divergence not only resulted in a European and an Asian *S. scrofa* clade, but also in differences in demographic history and population size. The last glacial maximum probably reduced population sizes of both European and Asian

was successfully domesticated [25].

formation.

24 Animal Domestication

**3.2. Divergence between European and Asian** *S. scrofa*

The demographic and geographic history of the domesticated pig may be just as complex as that of its wild counterpart. There is compelling evidence that pig domestication events occurred at multiple locations, Eastern Anatolia and China independently, some 9000–10,000 years ago [26, 37]. Domestication has not been a single event, but rather a long period with recurrent admixture with wild populations [38]. Following initial domestication, the traits selected as well as how animals were kept, strongly differed in Europe and Asia resulting in highly different domesticated pigs between Europe and Asia. Asian pigs were kept in close proximity of humans, often integrated in their settlements. By contrast, European pigs were roaming freely in forested areas in the surroundings [39, 40]. Only during the Industrial Revolution, a more strict pig farming system was adopted and implemented to fulfill the increasing demand for pork. Because of recurrent gene-flow between wild and domestic pigs, a reduction in genetic diversity cannot be observed in domesticated pigs compared to their presumed wild counterparts [35, 38, 41]. One should realize though that European and Asian domesticated pigs have been geographically isolated for over a million years ago, because they have distinct wild origins. Therefore, they genetically resemble local wild boar more than domestic pigs from different geographic origins [24, 35]. This dichotomy also underlies the fact that European pigs and wild boar are genetically less diverse than Asian wild boar and domestic pigs.

#### **3.4. Hybridization between domesticated pigs of different origin**

It is well documented that during the Industrial Revolution in Europe, European pigs have been deliberately hybridized with Asian pigs. Urbanization in Europe increased the demand for meat such as pork, but during those times, pig farmers would still have their pigs roaming in surrounding forests. Forest cover was decreasing and a different pig production system seemed inevitable [40]. Due to this changing environment, pig breeders sought a way to improve their stock in such way that pigs had to become adapted to living in small(er) enclosures, be more prolific and gain weight more rapidly. This led to selection for traits better adapted to the changed environment. Many of these traits were already present in Asian domestic pigs. Therefore, British farmers started crossbreeding their own pigs with these Asian pigs [40]. This introgression of Asian genetic material into European populations has long been demonstrated by genetic markers [42, 43]. Moreover, the intentional crossbreeding and consecutive artificial selection on Asia-derived traits enabled adaptive loci to emerge in the genome of European domestic pigs. Genes of Asian origin have been demonstrated to contribute to increased fertility and fatness in commercial Large White pigs [44, 45]. Very recently, hybridization between wild and domesticated pigs has been reported in Western Europe, resulting in traceable Asian genetic material in local wild boar populations in Germany [31, 32, 34].

genomic architecture of a species. In cattle, for example, exchange of genetic material between different species promoted the uptake of beneficial traits from closely related species [53]. In pig, domestication does not seem to have left a clear population bottleneck, as demonstrated by the high level of genetic variation in European pigs [38]. This suggests that the majority of the genetic variation that is present in European wild boar is also present in domestic breeds, even though modern pigs are phenotypically clearly different from their wild counterparts. Moreover, the gene-flow with wild populations as well as between different domestic lineages enabled pig breeders to select for locally and globally preferred traits, using a broad genetic background [44, 45]. Remarkably, the extensive mixture of genetic material leading towards the current European commercial pigs has resulted in domestic breeds that are genetically more diverse than their wild ancestors in Europe [24, 35, 36, 41]. This counter-intuitive characteristic of commercial pigs is mainly driven by the influx of Asian genes during the Industrial Revolution [45]; local heritage breeds that do not display signs of Asian gene-flow tend to have lower genetic diversity [50, 51]. Nowadays, many breeds and definitions are used to describe the origin of (local) stock, with some being a complex mixture of Asian and European heritage, depending on the geographical region and the breeding

A Genomics Perspective on Pig Domestication http://dx.doi.org/10.5772/intechopen.82646 27

Pig farming has drastically changed since first domestication. Todays' elaborate pig breeding industry has only few characteristics in common with early pig farmers, and has resulted in a highly professional large-scale pork production system, making use of latest technologies in animal breeding. Selection for particular traits not only improved due to more precise phenotyping and better defined traits such as carcass quality, growth rate and fertility [54], but also because of crossing breeds with desirable traits of different origins [45]. The use of pedigree information and large-scale tracking of animal relatedness has speeded up the improvement of pig breeds. In other livestock, especially cattle, the implementation of the use of genetic markers on top of pedigree information resulted in even more efficient selection [55]. The recent and rapid genetic progress can be achieved due to the implementation of genomic selection, in which animals are selected based on their performance predicted from their genotypes, rather than phenotypes [56]. This way, animals can be selected at an earlier stage, and predicted phenotypes for typically female traits can also be implemented using

Genomics has not only proven useful as a tool in genomic selection, but also has provided more understanding about the molecular mechanisms that underlie traits of interest. Knowledge about the link between genes and trait enables more accurate breeding [54]. Moreover, if the function of a specific gene is known, it can provide insight into the selection history of a breed. Numerous studies have successfully identified selection for genes linked to specific commercially important traits (**Table 1**). Interestingly, some of these genes under selection in European breeds have an Asian origin [59–61]. Also, genome-wide scans for detrimental variants have identified mutations in commercial populations with negative effects [62, 63].

practice of pig farmers.

**5. Breeding and genomics go hand in hand**

genotype information from males [57, 58].

#### **3.5. Breed formation and globalization**

Due to the worldwide consumption of pork, the species is farmed at a global scale, far exceeding its original natural distribution (IUCN). The influence and contribution of commercial pig breeds to local ecology and biodiversity is however debated [31, 32, 46]. Also, escape or intentional release of local stocks have resulted in feralization of domesticated pigs, which is now a major population in the United States, although the continent is not part of the native range of the species [47]. The domesticated pig as it is used nowadays for agricultural purposes consists of many breeds that have been separated and kept isolated for decades, which has resulted in many genetic differences between these breeds. Breed and population specific genetic studies have greatly enhanced the dissection of complex traits that are economically important. Knowing and understanding the origin and distribution of variation in (domesticated) species is important for conservation of genetic resources, such as culturally important heritage breeds [48]. Local husbandry and breeding techniques have created an enormous diversification of pig breeds. Generally, European breeds can be categorized into global commercial breeds, stemming from the White type in England, and local heritage breeds, developed locally and now often endangered [39]. It is notable that many heritage breeds genetically resemble the local wild boar more than global pig breeds, most likely because they were not improved by Asian gene-flow two centuries ago [35, 49–51]. The globalization of pig breeding and consumption has swamped local pig breeds with common commercial breeds from British heritage background, such as Large White, Landrace, Pietrain and Duroc [39]. Also, extensive admixture between breeds of different origin is known to occur, highly dependent on local breeding practices.

### **4. The hybrid nature of (pig) genomes**

Increasing evidence showed that humans play an important role in stimulating hybridization in wild species, either unintentionally or on purpose. Human-induced hybridization can not only be a by-product of globalization as some species became widely distributed due to human mobility, but it can also be intentional such as in domesticated species [40, 52]. It is becoming apparent that many livestock species/breeds are actually a mixture of highly divergent populations with a mixed demographic history, combined in one genome. The formation of livestock breeds provides a good example of how man has influenced the genomic architecture of a species. In cattle, for example, exchange of genetic material between different species promoted the uptake of beneficial traits from closely related species [53]. In pig, domestication does not seem to have left a clear population bottleneck, as demonstrated by the high level of genetic variation in European pigs [38]. This suggests that the majority of the genetic variation that is present in European wild boar is also present in domestic breeds, even though modern pigs are phenotypically clearly different from their wild counterparts. Moreover, the gene-flow with wild populations as well as between different domestic lineages enabled pig breeders to select for locally and globally preferred traits, using a broad genetic background [44, 45]. Remarkably, the extensive mixture of genetic material leading towards the current European commercial pigs has resulted in domestic breeds that are genetically more diverse than their wild ancestors in Europe [24, 35, 36, 41]. This counter-intuitive characteristic of commercial pigs is mainly driven by the influx of Asian genes during the Industrial Revolution [45]; local heritage breeds that do not display signs of Asian gene-flow tend to have lower genetic diversity [50, 51]. Nowadays, many breeds and definitions are used to describe the origin of (local) stock, with some being a complex mixture of Asian and European heritage, depending on the geographical region and the breeding practice of pig farmers.

#### **5. Breeding and genomics go hand in hand**

the changed environment. Many of these traits were already present in Asian domestic pigs. Therefore, British farmers started crossbreeding their own pigs with these Asian pigs [40]. This introgression of Asian genetic material into European populations has long been demonstrated by genetic markers [42, 43]. Moreover, the intentional crossbreeding and consecutive artificial selection on Asia-derived traits enabled adaptive loci to emerge in the genome of European domestic pigs. Genes of Asian origin have been demonstrated to contribute to increased fertility and fatness in commercial Large White pigs [44, 45]. Very recently, hybridization between wild and domesticated pigs has been reported in Western Europe, resulting in traceable Asian

Due to the worldwide consumption of pork, the species is farmed at a global scale, far exceeding its original natural distribution (IUCN). The influence and contribution of commercial pig breeds to local ecology and biodiversity is however debated [31, 32, 46]. Also, escape or intentional release of local stocks have resulted in feralization of domesticated pigs, which is now a major population in the United States, although the continent is not part of the native range of the species [47]. The domesticated pig as it is used nowadays for agricultural purposes consists of many breeds that have been separated and kept isolated for decades, which has resulted in many genetic differences between these breeds. Breed and population specific genetic studies have greatly enhanced the dissection of complex traits that are economically important. Knowing and understanding the origin and distribution of variation in (domesticated) species is important for conservation of genetic resources, such as culturally important heritage breeds [48]. Local husbandry and breeding techniques have created an enormous diversification of pig breeds. Generally, European breeds can be categorized into global commercial breeds, stemming from the White type in England, and local heritage breeds, developed locally and now often endangered [39]. It is notable that many heritage breeds genetically resemble the local wild boar more than global pig breeds, most likely because they were not improved by Asian gene-flow two centuries ago [35, 49–51]. The globalization of pig breeding and consumption has swamped local pig breeds with common commercial breeds from British heritage background, such as Large White, Landrace, Pietrain and Duroc [39]. Also, extensive admixture between breeds of different origin is known to occur, highly dependent on local

Increasing evidence showed that humans play an important role in stimulating hybridization in wild species, either unintentionally or on purpose. Human-induced hybridization can not only be a by-product of globalization as some species became widely distributed due to human mobility, but it can also be intentional such as in domesticated species [40, 52]. It is becoming apparent that many livestock species/breeds are actually a mixture of highly divergent populations with a mixed demographic history, combined in one genome. The formation of livestock breeds provides a good example of how man has influenced the

genetic material in local wild boar populations in Germany [31, 32, 34].

**3.5. Breed formation and globalization**

26 Animal Domestication

breeding practices.

**4. The hybrid nature of (pig) genomes**

Pig farming has drastically changed since first domestication. Todays' elaborate pig breeding industry has only few characteristics in common with early pig farmers, and has resulted in a highly professional large-scale pork production system, making use of latest technologies in animal breeding. Selection for particular traits not only improved due to more precise phenotyping and better defined traits such as carcass quality, growth rate and fertility [54], but also because of crossing breeds with desirable traits of different origins [45]. The use of pedigree information and large-scale tracking of animal relatedness has speeded up the improvement of pig breeds. In other livestock, especially cattle, the implementation of the use of genetic markers on top of pedigree information resulted in even more efficient selection [55]. The recent and rapid genetic progress can be achieved due to the implementation of genomic selection, in which animals are selected based on their performance predicted from their genotypes, rather than phenotypes [56]. This way, animals can be selected at an earlier stage, and predicted phenotypes for typically female traits can also be implemented using genotype information from males [57, 58].

Genomics has not only proven useful as a tool in genomic selection, but also has provided more understanding about the molecular mechanisms that underlie traits of interest. Knowledge about the link between genes and trait enables more accurate breeding [54]. Moreover, if the function of a specific gene is known, it can provide insight into the selection history of a breed. Numerous studies have successfully identified selection for genes linked to specific commercially important traits (**Table 1**). Interestingly, some of these genes under selection in European breeds have an Asian origin [59–61]. Also, genome-wide scans for detrimental variants have identified mutations in commercial populations with negative effects [62, 63].


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A Genomics Perspective on Pig Domestication http://dx.doi.org/10.5772/intechopen.82646 29

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**Table 1.** Non-exhaustive list of genes associated with commercially important traits in pigs.

Recent work demonstrates that some variants that cause lethality in homozygous state are present at relatively high frequency in commercial pig lines [64, 65]. Knowing these recessive lethal mutations can aid in avoiding matings between carriers of such mutations within the breeding scheme. Overall, genomics has provided valuable insight into variation in pigs: what its origin is, how is it maintained, reduced and increased. This turned out to be a complex interplay of molecular processes, selection, demographic history, gene-flow and human interference. Moreover, genomics is an important tool in the pig industry nowadays and is integral to modern commercial breeding.

### **Author details**

#### Mirte Bosse1,2\*

\*Address all correspondence to: mirte.bosse@wur.nl

1 Wageningen University & Research – Animal Breeding and Genomics, Wageningen, The Netherlands

2 VU University Amsterdam – Animal Ecology, Amsterdam, The Netherlands

#### **References**

Recent work demonstrates that some variants that cause lethality in homozygous state are present at relatively high frequency in commercial pig lines [64, 65]. Knowing these recessive lethal mutations can aid in avoiding matings between carriers of such mutations within the breeding scheme. Overall, genomics has provided valuable insight into variation in pigs: what its origin is, how is it maintained, reduced and increased. This turned out to be a complex interplay of molecular processes, selection, demographic history, gene-flow and human interference. Moreover, genomics is an important tool in the pig industry nowadays and is

**Table 1.** Non-exhaustive list of genes associated with commercially important traits in pigs.

1 Wageningen University & Research – Animal Breeding and Genomics, Wageningen,

2 VU University Amsterdam – Animal Ecology, Amsterdam, The Netherlands

integral to modern commercial breeding.

**Gene Trait Study**

28 Animal Domestication

*KIT* Coat color Andersson and Plastow [66]

*MC1R* Coat color Kijas et al., [67]; Fang et al., [68] *EDNRB* Coat color Ai et al., [59]; Wilkinson et al., [69]

*KITLG* Coat color Okumura et al., [61]

*IGF2* Lean growth van Laere et al., [70] *RYR1* Lean growth Fujii et al., [71] *PRKAG3* Lean growth Milan et al., [72] *NR6A1* Body size Rubin et al., [73] *PLAG1* Body size Rubin et al., [73] *LCORL* Body size Rubin et al., [73] *OSTN* Body composition Rubin et al., [73] *CLDN1* Fertility Choi et al., [74] *AHR* Fertility Bosse et al., [44] *TWIST1* Fatness Choi et al., [74] *LEMD3* Ear morphology Wilkinson et al., [59]

\*Address all correspondence to: mirte.bosse@wur.nl

**Author details**

Mirte Bosse1,2\*

The Netherlands


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A Genomics Perspective on Pig Domestication http://dx.doi.org/10.5772/intechopen.82646 31

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**Chapter 3**

**Provisional chapter**

**Insects: The Disregarded Domestication Histories**

**Insects: The Disregarded Domestication Histories**

DOI: 10.5772/intechopen.81834

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 humandirected pathway and domestication syndrome (e.g., increased tameness, decreased

aggressiveness, modified reproduction) between several insect species.

**Keywords:** domestication level, domestication pathways, domestication syndrome,

Domestication is one of the most important developments in human history [1]. 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, 4–6]. 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

> © 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,

distribution, and reproduction in any medium, provided the original work is properly cited.

Additional information is available at the end of the chapter

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.81834

Thomas Lecocq

Thomas Lecocq

**Abstract**

insect species

**1. Introduction**


#### **Insects: The Disregarded Domestication Histories Insects: The Disregarded Domestication Histories**

DOI: 10.5772/intechopen.81834

#### Thomas Lecocq Thomas Lecocq

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34 Animal Domestication

Nature. 2003;**425**:832-836

1991;**253**:448-451

**288**:1248-1251

Additional information is available at the end of the chapter Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.81834

**Abstract**

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 humandirected pathway and domestication syndrome (e.g., increased tameness, decreased aggressiveness, modified reproduction) between several insect species.

**Keywords:** domestication level, domestication pathways, domestication syndrome, insect species

#### **1. Introduction**

Domestication is one of the most important developments in human history [1]. 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, 4–6]. 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

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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 [9–11].

The notions of domesticated species and domestication process are among the most confusing and controversial concepts in biology [12–14]. 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 [1]. Nevertheless, there were some attempts to unify the alternative points of view to some extent [1, 12, 13, 15–17]. 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, 15–17]. 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 [12]. 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 [12]. These environments can be captive or "ranch" conditions quite isolated from wild populations where living conditions, diet, and food are controlled by humans [19]. 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., [20]); 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 [21]; level 4—the life cycle is fully controlled by humans in man-controlled environments without wild inputs [12]. 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., [22–24]). 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 [10]. 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

**Figure 1.** Domestication process and insect domestication level. Numbers 0–5 refer to the domestication levels [12, 18]. Characteristics of each domestication level are provided on the left. Lines and points near the insect species names show

Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 37

the range of domestication degrees observed among populations of the species.

#### Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 37

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 spe-

The notions of domesticated species and domestication process are among the most confusing and controversial concepts in biology [12–14]. 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 [1]. Nevertheless, there were some attempts to unify the alternative points of view to some extent [1, 12, 13, 15–17]. 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, 15–17]. 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 [12]. 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 [12]. These environments can be captive or "ranch" conditions quite isolated from wild populations where living conditions, diet, and food are controlled by humans [19]. 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., [20]); 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 [21]; level 4—the life cycle is fully controlled by humans in man-controlled environments without wild inputs [12]. 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., [22–24]). 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

cies notion, or the domestication histories still remain [9–11].

36 Animal Domestication

**Figure 1.** Domestication process and insect domestication level. Numbers 0–5 refer to the domestication levels [12, 18]. Characteristics of each domestication level are provided on the left. Lines and points near the insect species names show the range of domestication degrees observed among populations of the species.

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 [10]. 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 [26]. 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 [26]. Most modern domestic species such as pets [27], transport animals [10], and aquatic species [12, 28] have arisen because of this pathway [10]. 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]).

[50, 51]. Although silk has a tiny percentage of the global textile fiber market (i.e., less than 0.2%; the yearly worldwide production is about 200,000 metric tons of silk [51]), the annual turnover of the China National Silk Import and Export Corporation alone is more than 2 billion US\$ [19, 51]. Moreover, silk production provides employments to several million persons in rural and semirural areas across the world [19] (e.g., 8 millions in India [51]). Beside its economic importance, *B. mori* is an edible insect [19], a health food [19], a pet [19], and model species for basic research because of its short life cycle and adaptation to laboratory culture [52–55].

Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 39

The silkworm life cycle is strongly controlled by humans in indoor facilities with controlled environmental conditions [51]. 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) [51]. 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) [51]. After several molts, caterpillars climb on man-provided supports and spin their silken cocoons. Then, cocoons are collected and *B. mori* specimens are killed before metamorphosis since proteolytic enzymes released to make a hole in the cocoon by the adults are destructive to the silk [51]. Some cocoons are allowed to survive in order to produce adults for breeding [51]. In contrast to closely related wild moth species (e.g., *B. mandarina*) that fly for reproduction or evasion from predators, *B. mori* adults are not capable of functional flight due to their too big/heavy body and their small wings [51]. Therefore, *B. mori* completely relies on human assistance in finding a mate and a laying support [51]. The *B. mori* oviposition site selection is also controlled by humans (i.e., egg laying occurs on man-

*Bombyx mori* is one of the few insects commonly acknowledged as truly domesticated and as a stunning case in point of insect domestication [47, 52, 57, 58]. Several archeological and molecular studies have tried to trace the history of its domestication (e.g., [57, 59–62]). The silkworm was domesticated roughly 7500 years ago from Chinese populations of *B. mandarina*, an extant wild silk moth of East Asia [57, 59, 60, 63]. The domestication of the silkworm is thought to be a directed pathway [10] starting at a single event [61]. Long-term bidirectional significant gene flow occurred between wild and domesticated silkworm populations during the first 3500 years of the domestication [59] most likely because of accidental escapes and intentional hybridizations by breeders to produce desirable strains [52, 59, 64]. Nowadays,

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 [57]. Indeed, the opening of Silk Road has dramatically impacted

**2.1.** *Bombyx mori* **life cycle and production**

offered mulberry plant or on filter paper) [51, 56].

**2.2. Domestication history and pathway of** *Bombyx mori*

low gene flow presumably still exists with *B. mandarina* [65].

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, 31–34]. 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 [35–40]. 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) [35]. 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 [10]. 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 [46]. However, insects' domestication has comparatively received far less attention to date [47]. 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 mori* (Lepidoptera, Bombycidae). It is one of the most important insects in human economy because the species is the primary producer of silk [50, 51]. Although silk has a tiny percentage of the global textile fiber market (i.e., less than 0.2%; the yearly worldwide production is about 200,000 metric tons of silk [51]), the annual turnover of the China National Silk Import and Export Corporation alone is more than 2 billion US\$ [19, 51]. Moreover, silk production provides employments to several million persons in rural and semirural areas across the world [19] (e.g., 8 millions in India [51]). Beside its economic importance, *B. mori* is an edible insect [19], a health food [19], a pet [19], and model species for basic research because of its short life cycle and adaptation to laboratory culture [52–55].

#### **2.1.** *Bombyx mori* **life cycle and production**

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 [26]. 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 [26]. Most modern domestic species such as pets [27], transport animals [10], and aquatic species [12, 28] have arisen because of this pathway [10]. 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]).

38 Animal Domestication

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, 31–34]. 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 [35–40]. 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) [35]. 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 [10]. 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 [46]. However, insects' domestication has comparatively received far less attention to date [47]. 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.

Silkworm is the caterpillar of the moth *Bombyx mori* (Lepidoptera, Bombycidae). It is one of the most important insects in human economy because the species is the primary producer of silk

**2. The silkworm and the sericulture**

The silkworm life cycle is strongly controlled by humans in indoor facilities with controlled environmental conditions [51]. 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) [51]. 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) [51]. After several molts, caterpillars climb on man-provided supports and spin their silken cocoons. Then, cocoons are collected and *B. mori* specimens are killed before metamorphosis since proteolytic enzymes released to make a hole in the cocoon by the adults are destructive to the silk [51]. Some cocoons are allowed to survive in order to produce adults for breeding [51]. In contrast to closely related wild moth species (e.g., *B. mandarina*) that fly for reproduction or evasion from predators, *B. mori* adults are not capable of functional flight due to their too big/heavy body and their small wings [51]. Therefore, *B. mori* completely relies on human assistance in finding a mate and a laying support [51]. The *B. mori* oviposition site selection is also controlled by humans (i.e., egg laying occurs on manoffered mulberry plant or on filter paper) [51, 56].

#### **2.2. Domestication history and pathway of** *Bombyx mori*

*Bombyx mori* is one of the few insects commonly acknowledged as truly domesticated and as a stunning case in point of insect domestication [47, 52, 57, 58]. Several archeological and molecular studies have tried to trace the history of its domestication (e.g., [57, 59–62]). The silkworm was domesticated roughly 7500 years ago from Chinese populations of *B. mandarina*, an extant wild silk moth of East Asia [57, 59, 60, 63]. The domestication of the silkworm is thought to be a directed pathway [10] starting at a single event [61]. Long-term bidirectional significant gene flow occurred between wild and domesticated silkworm populations during the first 3500 years of the domestication [59] most likely because of accidental escapes and intentional hybridizations by breeders to produce desirable strains [52, 59, 64]. Nowadays, low gene flow presumably still exists with *B. mandarina* [65].

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 [57]. 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 [51].

Although other species like *A. dorsata* or *A. cerana* can be important for human economy and feeding in certain countries, none achieves the crucial economic, agricultural, scientific, and environmental importance of *A. mellifera* [89–91]. Its importance relies on its pollination activity as well as on its production of honey, wax, venom, pollen pellets, propolis, and royal jelly [92].

Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 41

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 [75]. 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 [75]. 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 [94]. 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 [89]. In the old nest, new queens compete until only one remains and the survivor takes the nest control [89]. Then, the new queen goes on one or more nuptial flights and mates with several drones [95]. Once mating is done, the queen remains in the hive and lays eggs [89]. 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 [89]. 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

Molecular dating suggests that *A. mellifera* expanded its distribution around 1 million years ago [98, 99] from a still debated ancestral range [76, 90, 98–102]. During its range expansion, the western honey bee experienced local adaptations [103] and geographic differentiations leading to the current substantial phenotypic variation across its extensive geographic range [101]. This intraspecific variability has been used to develop an extensive classification of 29 subspecies (or "races") [76]. These taxa are now lumped into four major groups based on morphological, genetical, ecological, physiological, and behavioral traits: the African, Western/ Northern European, Eastern European, and Middle East populations (review in [100]). The European groups exhibit phenotypic adaptations to survive colder winters, whereas the

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

African group is more aggressive and shows a greater tendency to swarm [101].

**3.1.** *Apis mellifera* **life cycle and production**

controlling mating by artificial insemination [96, 97].

**3.2. Domestication history, traits, and pathway of** *Apis mellifera*

#### **2.3. Consequences and progress of the domestication process in** *Bombyx mori*

*Bombyx mori* displays significant specificities compared to its phylogenetically nearest wild counterpart [67–71]. Some of these traits can be considered as (i) domestication traits reinforced by or (ii) improvement traits fostered by selective pressures shaped by unintentional/ deliberate human actions and human-modified environments: an increased cocoon size, larger body size, higher silk production, higher growth rate, larger tolerance to human presence/ handling, higher ability to live in crowded conditions, and a better feed efficiency [51, 52, 57]. Conversely, other specificities could be explained by a relaxation of the selection occurring in the wild (e.g., predation pressure): leucism (meaning the loss of camouflage) and disability to fly [51, 68]. These last changes have made *B. mori* entirely dependent upon humans for survival, feeding, and reproduction [51, 52]. Moreover, independent selective breeding programs and different breeding environments (i.e., from temperate to tropical climate) have led to the development of more than 1000 inbred lines or strains of domesticated silkworms across the world [51, 57, 60, 72]. Since *B. mori* (i) has its life cycle fully controlled by humans in captivity, (ii) is entirely dependent on humans for reproduction, (ii) and undergoes selective breeding and genetic improvement to harvest maximum output, they are one of the few insect species at a very advanced domestication stage (Level 5; **Figure 1**). While they are not as extreme as the *B. mori* case, other moth species used for silk production have their life cycle under human control and dependence such as *Samia cynthia* (i.e., ericulture; see [73, 74]).

#### **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 [75]. They belong to the same genus (Hymenoptera, Apidae, *Apis* spp.) that includes 11 species and many subspecies native from the Old World [75, 76]. The dwarf honey bees (*A. florea* and *A. andreniformis*) are small species from southern and southeastern Asia that make small open nests in trees and shrubs [75, 77, 78]. These species produce honey that is harvested and eaten by local human populations [77, 79]. The giant honey bees (*A. binghami*, *A. breviligula*, *A. dorsata*, and *A. laboriosa*) are aggressive species inhabiting forest areas of South and Southeast Asia [80–82]. They produce honey and wax in their open nest on trees, cliffs, or buildings that are harvested by indigenous people [83–85]. *Apis koschevnikovi* and *A.nuluensis* are cavity-nesting species that occur in the tropical evergreen forests of Borneo [86, 87]. *Apis nigrocincta* is a cavity-nesting species reported in Sulawesi [75]. The western honey bee (*A. mellifera*) and the eastern honey bee (*A. cerana*) are cavity-nesting species native throughout (i) Africa, the Middle East, and Europe and (ii) South and Southeast Asia, respectively [75]. All *Apis* species are important pollinators for many ecosystems [88]. Although other species like *A. dorsata* or *A. cerana* can be important for human economy and feeding in certain countries, none achieves the crucial economic, agricultural, scientific, and environmental importance of *A. mellifera* [89–91]. Its importance relies on its pollination activity as well as on its production of honey, wax, venom, pollen pellets, propolis, and royal jelly [92].

#### **3.1.** *Apis mellifera* **life cycle and production**

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

*Bombyx mori* displays significant specificities compared to its phylogenetically nearest wild counterpart [67–71]. Some of these traits can be considered as (i) domestication traits reinforced by or (ii) improvement traits fostered by selective pressures shaped by unintentional/ deliberate human actions and human-modified environments: an increased cocoon size, larger body size, higher silk production, higher growth rate, larger tolerance to human presence/ handling, higher ability to live in crowded conditions, and a better feed efficiency [51, 52, 57]. Conversely, other specificities could be explained by a relaxation of the selection occurring in the wild (e.g., predation pressure): leucism (meaning the loss of camouflage) and disability to fly [51, 68]. These last changes have made *B. mori* entirely dependent upon humans for survival, feeding, and reproduction [51, 52]. Moreover, independent selective breeding programs and different breeding environments (i.e., from temperate to tropical climate) have led to the development of more than 1000 inbred lines or strains of domesticated silkworms across the world [51, 57, 60, 72]. Since *B. mori* (i) has its life cycle fully controlled by humans in captivity, (ii) is entirely dependent on humans for reproduction, (ii) and undergoes selective breeding and genetic improvement to harvest maximum output, they are one of the few insect species at a very advanced domestication stage (Level 5; **Figure 1**). While they are not as extreme as the *B. mori* case, other moth species used for silk production have their life cycle under human

silkworm disease breakouts and the raising of cotton industry [51].

40 Animal Domestication

**2.3. Consequences and progress of the domestication process in** *Bombyx mori*

control and dependence such as *Samia cynthia* (i.e., ericulture; see [73, 74]).

Honey bees are eusocial insect species distinguished by their production and storage of honey and their construction of colonial nests from wax [75]. They belong to the same genus (Hymenoptera, Apidae, *Apis* spp.) that includes 11 species and many subspecies native from the Old World [75, 76]. The dwarf honey bees (*A. florea* and *A. andreniformis*) are small species from southern and southeastern Asia that make small open nests in trees and shrubs [75, 77, 78]. These species produce honey that is harvested and eaten by local human populations [77, 79]. The giant honey bees (*A. binghami*, *A. breviligula*, *A. dorsata*, and *A. laboriosa*) are aggressive species inhabiting forest areas of South and Southeast Asia [80–82]. They produce honey and wax in their open nest on trees, cliffs, or buildings that are harvested by indigenous people [83–85]. *Apis koschevnikovi* and *A.nuluensis* are cavity-nesting species that occur in the tropical evergreen forests of Borneo [86, 87]. *Apis nigrocincta* is a cavity-nesting species reported in Sulawesi [75]. The western honey bee (*A. mellifera*) and the eastern honey bee (*A. cerana*) are cavity-nesting species native throughout (i) Africa, the Middle East, and Europe and (ii) South and Southeast Asia, respectively [75]. All *Apis* species are important pollinators for many ecosystems [88].

**3. The honey bees: beekeeping or apiculture?**

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 [75]. 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 [75]. 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 [94]. 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 [89]. In the old nest, new queens compete until only one remains and the survivor takes the nest control [89]. Then, the new queen goes on one or more nuptial flights and mates with several drones [95]. Once mating is done, the queen remains in the hive and lays eggs [89]. 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 [89]. 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** *Apis mellifera*

Molecular dating suggests that *A. mellifera* expanded its distribution around 1 million years ago [98, 99] from a still debated ancestral range [76, 90, 98–102]. During its range expansion, the western honey bee experienced local adaptations [103] and geographic differentiations leading to the current substantial phenotypic variation across its extensive geographic range [101]. This intraspecific variability has been used to develop an extensive classification of 29 subspecies (or "races") [76]. These taxa are now lumped into four major groups based on morphological, genetical, ecological, physiological, and behavioral traits: the African, Western/ Northern European, Eastern European, and Middle East populations (review in [100]). The European groups exhibit phenotypic adaptations to survive colder winters, whereas the African group is more aggressive and shows a greater tendency to swarm [101].

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 [106]. 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 [105]. 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 [105]. Over time, humans increased their control on bees by developing swarming control device (i.e., queen excluder [96]), reproduction control (e.g., artificial insemination [97]), mass breeding (e.g., [107]), selective breeding programs (e.g., [108–110]), and new strains (e.g., Buckfast strain [111] or Africanized honey bees [112]).

deadly competition between them [121]), decreased aggressiveness, higher honey production, increased foraging zeal, and disinclination to swarm of some strains [111]. These specificities can be interpreted as improvement traits within a domestication syndrome. Second, many other species acknowledged as "domesticated" can survive in the wild (e.g., feral populations of rabbits, cats, and dogs [122]; although fast initial decline in fitness of domesticated escapees in the wild is expected [123]). Moreover, the ability of honey bees to survive in the wild could be overestimated since most *A. mellifera* are not considered to be self-sustaining as veterinary treatments against the mite *Varroa destructor* among other parasites is often provided [120]. Third, gene flow between "nonwild" and wild populations is commonly observed during the domestication process (see [21, 124, 125]). Actually, the debate about the status of domesticated animal for *A. mellifera* exemplifies the subjectivity of the domestic species threshold. Beside this controversial definition, *A. mellifera* shows that different conspecific populations can be at different stages of the domestication process. Indeed, there is no control by humans over the life cycle of wild populations that are commonly observed for the African group [126–128]. In contrast, many populations belonging to the European groups have a life cycle completed in man-made environment (i.e., hives) and controlled by humans (i.e., control of superorganism reproduction), feed on domesticated crops (i.e., humans can actively control the honey bee food supply for honey production or crop pollination) and/or on artificial food provided by humans (i.e., sugar syrup) [129], and some of them undergo selective breeding programs [108–111]. Therefore, the domestication levels of *A. mellifera* range from 0 to 5 according to the population considered.

Insects: The Disregarded Domestication Histories http://dx.doi.org/10.5772/intechopen.81834 43

**4. The bumble bees and the stingless bees: the other bee** 

About 90% of world's plant species are pollinated by animals [130–132], and the main animal pollinators in most ecosystems are bees [88]. 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 *A. mellifera* to breed a strain of bees that would produce more honey and be better adapted to tropical conditions) in Neotropics [138], and the poor pollination efficiency of *A. mellifera* for some plants, as well as the requirement of maintaining the honey bee colonies outside the flowering period of valuable crops [139] have triggered or restarted the domestication of other bee species: the bumble bees and the stingless bees.

Bumble bees (Hymenoptera, Apidae, *Bombus* spp.) are social insects with a nearly worldwide distribution with their largest species diversity in temperate and cold areas [75, 140]. Except in

**domestications**

**4.1. The bumble bees**

The honey bees' domestication concerns only *A. mellifera* and *A. cerana* (see details about the later species in [89]) most likely because they display intrinsic features that facilitated the domestication process: (i) cavity-nesting habit making hives suitable for these species, (ii) hygienic behavior (i.e., detection and removal of diseased brood and wastes) limiting diseases, and (iii) adaptations to tropical and temperate climate facilitating the apiculture development across the world [89, 110], for example, *A. mellifera*. Moreover, differentiations in traits facilitating beekeeping are observed at the subspecies level. Subsequently, some particular subspecies were preferably domesticated by humans. For instance, non-African subspecies have been more widely used by most beekeepers since they can survive in temperate regions, have a low tendency to swarm, and low aggressiveness [101].

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 [10], 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].

#### **3.3. Is** *Apis mellifera* **domesticated?**

Many authors acknowledge (often without justification) the domesticated status of *A. mellifera* (e.g., [10, 16, 47, 58, 89, 102, 115–117]). In contrast, *A. mellifera* has been considered as never properly domesticated but only as managed species by other authors (e.g., [110, 114]; however, some of these scientists acknowledge an ongoing domestication process) because (i) their biology, physiology, and behavior are seen as largely unchanged from their wild counterparts [114], (ii) honey bees are able to survive without human's help [118], (iii) there is extensive gene flow between wild/feral and managed bees in native range due to the difficulties to achieve controlled mating [119]. However, these points should be reconsidered. First, the comparison of phenotypes between "wild" and "nonwild" populations is difficult in a large a part of the species range. Indeed, colonies that are found in the wild may have escaped from a managed colony, and therefore, they may not be wild [120]. In Europe, it is unlikely that there are any truly wild subpopulations left due to this gene flow [120]. This means that the differentiation fostered by the domestication process can be blurred by the large amount of feral populations in the wild. Nevertheless, there are significant behavioral changes observed in man-controlled honey bees stocks such as multiple queen colonies (i.e., colonies conserved several queens without deadly competition between them [121]), decreased aggressiveness, higher honey production, increased foraging zeal, and disinclination to swarm of some strains [111]. These specificities can be interpreted as improvement traits within a domestication syndrome. Second, many other species acknowledged as "domesticated" can survive in the wild (e.g., feral populations of rabbits, cats, and dogs [122]; although fast initial decline in fitness of domesticated escapees in the wild is expected [123]). Moreover, the ability of honey bees to survive in the wild could be overestimated since most *A. mellifera* are not considered to be self-sustaining as veterinary treatments against the mite *Varroa destructor* among other parasites is often provided [120]. Third, gene flow between "nonwild" and wild populations is commonly observed during the domestication process (see [21, 124, 125]). Actually, the debate about the status of domesticated animal for *A. mellifera* exemplifies the subjectivity of the domestic species threshold. Beside this controversial definition, *A. mellifera* shows that different conspecific populations can be at different stages of the domestication process. Indeed, there is no control by humans over the life cycle of wild populations that are commonly observed for the African group [126–128]. In contrast, many populations belonging to the European groups have a life cycle completed in man-made environment (i.e., hives) and controlled by humans (i.e., control of superorganism reproduction), feed on domesticated crops (i.e., humans can actively control the honey bee food supply for honey production or crop pollination) and/or on artificial food provided by humans (i.e., sugar syrup) [129], and some of them undergo selective breeding programs [108–111]. Therefore, the domestication levels of *A. mellifera* range from 0 to 5 according to the population considered.
