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The role of mitochondrial DNA to determine the origin of domestic chicken

Published online by Cambridge University Press:  03 June 2015

P. DI LORENZO ,
S. CECCOBELLI ,
F. PANELLA ,
G. ATTARD  and
E. LASAGNA
P. DI LORENZO
Affiliation:
Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università degli Studi di Perugia, Italy
S. CECCOBELLI
Affiliation:
Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università degli Studi di Perugia, Italy
F. PANELLA
Affiliation:
Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università degli Studi di Perugia, Italy
G. ATTARD
Affiliation:
Institute of Earth Systems, University of Malta, Malta
E. LASAGNA*
Affiliation:
Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università degli Studi di Perugia, Italy
*
Corresponding author: emiliano.lasagna@unipg.it

Abstract

Mitochondrial DNA (mtDNA) is has recently lost relevance especially when utilised to study species that are characterised with a history of several migrations. Nonetheless, mtDNA can still represents a useful additional tool in the study of molecular genetic diversity. The reason for the adoption of mtDNA is that it is easy to amplify because it appears in multiple copies in the cells and the mitochondrial gene content is strongly conserved across generations. Thousands of published studies have reached conclusions about population history, patterns of gene flow, genetic structure, and species limits, on the basis of mtDNA sequence variation. MtDNA has been used to study phylo-geographic structure of avian species, and to identify the number of maternal lineages and their geographic origins. Most studies of chicken mtDNA rely on sequences of partial control region but recent researches used the complete mtDNA genome to reconstruct the history of animal domestication. The first genetic study on mtDNA suggests that the Indochinese Red Junglefowl subspecies Gallus gallus gallus is the primary ancestor of the domestic chicken (Gallus gallus domesticus). Other studies showed that at least three subspecies of Gallus gallus were enrolled in the origin of domestic chicken breeds, and that there may be at least two domestication centres: one in Southeast Asia and one in the Indian subcontinent. The authors suggested nine highly divergent clades (named clade A-I) related to geographical distribution in a wide range of domestic chickens and Red Junglefowls across Eurasian regions. Understanding when chickens were transported out of domestication centres and the directions in which they were moved provides information about prehistoric human migration, trade routes and cultural diffusion. MtDNA has been used to infer regions of domestication and to identify the number of maternal lineages and their geographic origins in macroevolution studies.

Keywords

molecular markersmaternal lineagephylogeographic structureanimal domestication

Information

Type
Reviews
Information
World's Poultry Science Journal , Volume 71 , Issue 2 , June 2015 , pp. 311 - 318
Copyright
Copyright © World's Poultry Science Association 2015 

Introduction

The chicken has a long history of anthropomorphic usage in Southeast and East Asia, where it has been bred for entertainment and show (Macdonald and Blench, Reference MACDONALD and BLENCH2000). The origin and domestication of chickens has been of interest to people since at least Roman times (Storey et al., Reference STOREY, STEPHEN, BRYANT, CARSON, EMERY, DE FRANCE, HIGHAM, HUYNEN, INTOH, JONES, KIRCH, LADEFOGED, MCCOY, MORALES-MUNIZ, QUIROZ, REITZ, ROBINS, WALTER and MATISOO-SMITH2012). Based on archaeological and historical evidence the domestication of the fowl is thought to have occurred in multiple, independent centres. Archaeological research has identified centres of chicken domestication in India and China; both within the natural range of wild Junglefowl (Crawford, Reference CRAWFORD1990).

Chickens were likely domesticated from wild Red Junglefowl, though some have suggested possible genetic contributions from other Junglefowl species (Eriksson et al., Reference ERIKSSON, LARSON, GUNNARSSON, BED'HOM, TIXIER-BOICHARD, STRÖMSTEDT, WRIGHT, JUNGERIUS, VEREIJKEN, RANDI, JENSEN and ANDERSSON2008; Nishibori et al., Reference NISHIBORI, SHIMOGIRI, HAYASHI and YASUE2005). Darwin (Reference DARWIN1896) was the first to propose that all domestic fowls descended directly from one common ancestor; the Gallus Bankiva, or wild Junglefowl breed that originated in Eastern and Southern Asia. He came to this conclusion based on comparisons of morphology and progeny produced from crosses between various species of Gallus. The genus Gallus consists of four species, Red Junglefowl, Grey Junglefowl (Gallus sonnerati), Green Junglefowl (Gallus varius), and Ceylon Junglefowl (Gallus lafayetii) (Delacour, Reference DELACOUR1977; Sibley and Ahlquist, Reference SIBLEY and AHLQUIST1990; Johnsgard, Reference JOHNSGARD1999). Based on the morphological differences and geographical distributions, the Red Junglefowl is further subdivided into five subspecies, Gallus gallus gallus (Red Junglefowl gal), Gallus gallus spadicus (Red Junglefowl spa), Gallus gallus banchiva (Red Junglefowl ban), Gallus gallus jabouillei (Red Junglefowl jab), and Gallus gallus murgi (Red Junglefowl mur) (Johnsgard, Reference JOHNSGARD1999). Zoologists at the time of Darwin had reservations on giving consensus to the opinion that all our domestic chicken breeds owe their origin to the genus Gallus Bankiva; nonetheless it was acknowledged that a great majority of breeds known at the time are its descendants. With the advent of molecular biology techniques, DNA sequence-based phylogenetic analyses have been conducted. The most extensive of these DNA-based analyses examined the D-Loop region mitochondrial, and provided support for Darwin's conclusion that the chicken was established through domestication of Red Junglefowl (Fumihito et al., Reference FUMIHITO, MIYAKE, TAKADA, SHINGU, ENDO, GOJOBORI, KONDO and OHNO1996). This conclusion was supported by other studies using microsatellites DNA (Hillel et al., Reference HILLEL, GROENEN, TIXIER-BOICHARD, KOROL, DAVID, KIRZHNER, BURKE, BARRE-DIRIE, CROOIJMANS, ELO, FELDMAN, FREIDLIN, MÄKI-TANILA, OORTWIJN, THOMSON, VIGNAL, WIMMERS and WEIGEND2003) and a large number of D-loop sequences (Liu et al., Reference LIU, WU, YAO, MIAO, LUIKART, BAIG, BEJA-PEREIRA, DING, GOUNDER PALANICHAMY and ZHANG2006). Recently, the analysis of the entire mtDNA genome has demonstrated that domestic chickens and wild Junglefowl may have substantial gene flow and genetic admixture following the domestication. In other case, some domestic chickens might have become feral with their descendants living as wild fowl (Miao et al., Reference MIAO, PENG, WU, OUYANG, YANG, YU, LIANG, PIANCHOU, BEJA-PEREIRA, MITRA, PALANICHAMY, BAIG, CHAUDHURI, SHEN, KONG, MURPHY, YAO and ZHANG2013). The various investigative techniques described above, do not substitute each other, but rather come together as different tools that complement each other in their specific specialisations to unravel the riddle of the history of domestication.

Understanding when chickens were transported out of domestication centres and the directions in which they drifted provides information about prehistoric human migration patterns, trade routes and cultural diffusion (Thomson et al., Reference THOMSON, LEBRASSEUR, AUSTIN, HUNT, BURNEY, DENHAM, RAWLENCE, WOOD, GONGORA, FLINK, LINDERHOLM, DOBNEY, LARSON and COOPER2014). Possible interactions may be reconstructed by mapping the presence of chickens in archaeological assemblages (Storey et al., Reference STOREY, LADEFOGED and MATISOO-SMITH2008) using historical evidence (Peters, Reference PETERS1913; Crawford, Reference CRAWFORD1984) also thought the mtDNA application (Liu et al., Reference LIU, WU, YAO, MIAO, LUIKART, BAIG, BEJA-PEREIRA, DING, GOUNDER PALANICHAMY and ZHANG2006, Miao et al., Reference MIAO, PENG, WU, OUYANG, YANG, YU, LIANG, PIANCHOU, BEJA-PEREIRA, MITRA, PALANICHAMY, BAIG, CHAUDHURI, SHEN, KONG, MURPHY, YAO and ZHANG2013).

Mitochondrial DNA is a useful marker to trace back the origin of livestock species and has been widely used to reconstruct domestication patterns (Groeneveld et al., Reference GROENEVELD, LENSTRA, EDING, TORO, SCHERF, PILLING, NEGRINI, FINLAY, JIANLIN, GROENEVELD and WEIGEND2010). Microsatellites (SSR) and mitochondrial DNA (mtDNA) sequences have already proved to be useful for assessing genetic variability, while single nucleotide polymorphisms (SNPs) are becoming more and more popular due to their very density and availability of high throughput genotyping techniques. A combination of SSR and mtDNA markers is a complementary approach that combines the highly polymorphic microsatellites whose high mutation rates allow for small scale resolution of more recent demographic event with mtDNA which shed light on phylogeographic events dating back further in time (Feulner et al., Reference FEULNER, BIELFELDT, ZACHOS, BRADVAROVIC, ECKERT and HARTL2004). Microsatellites have been used to asses genetic diversity of a number of native chicken population in Africa (Leroy et al., Reference LEROY, KAYANG, YOUSSAO, YAPI-GNAORÉ, OSEI-AMPONSAH, N'GORAN, FOTSA, BENABDELJELI, BED'HOM, TIXIER-BOICHARD and ROGNON2012; Goraga et al., Reference GORAGA, WEIGEND and BROCKMANN2012; Eltanany et al., Reference ELTANANY, PHILIPP, WEIGEND and DISTL2011), Europe (Ceccobelli et al., Reference CECCOBELLI, DI LORENZO, LANCIONI, CASTELLINI, MONTEAGUDO IBÁÑEZ, SABBIONI, SARTI, WEIGEND and LASAGNA2013; Wilkinson et al., Reference WILKINSON, WIENER, TEVERSON, HALEY and HOCKING2012; Zanetti et al., Reference ZANETTI, DE MARCHI, ABBADI and CASSANDRO2011; Bodzsar et al., Reference BODZSAR, EDING, REVAY, HIDAS and WEIGEND2009) and Asia (Pham et al., Reference PHAM, BERTHOULY-SALAZAR, TRAN, CHANG, CROOIJMANS, LIN, HOANG, LEE, TIXIER-BOICHARD and CHEN2013; Cuc et al., Reference CUC, SIMIANER, EDING, TIEU, CUONG, WOLLNY, GROENEVELD and WEIGEND2010; Berthouly et al., Reference BERTHOULY, LEROY, VAN, THANH, BED'HOM, NGUYEN, VU, MONICAT, TIXIER-BOICHARD, VERRIER, MAILLARD and ROGNON2009; Ngo Thim et al., Reference NGO THIM, MUCHADEYI, BAULAIN, EDING, WEIGEND and WOLLNY2006). The first chicken genome sequence draft was completed in 2004 (International Chicken Consortium, 2004); its availability offers new opportunities in the evaluation of chicken genetic diversity using SNPs (Gholami et al., Reference GHOLAMI, ERBE, GÄRKE, PREISINGER, WEIGEND, WEIGEND and SIMIANER2014; Granevitze et al., Reference GRANEVITZE, DAVID, TWITO, WEIGEND, FELDMAN and HILLEL2014; Siwek et al., Reference SIWEK, WRAGG, SŁAWIŃSKA, MALEK, HANOTTE and MWACHARO2013; Groenen et al., Reference GROENEN, WAHLBERG, FOGLIO, CHENG, MEGENS, CROOIJMANS, BESNIER, LATHROP, MUIR, WONG, GUT and ANDERSSON2009; Muir et al., Reference MUIR, WONG, ZHANG, WANG, GROENEN, CROOIJMANS, MEGENSD, ZHANGE, OKIMOTOF, VEREIJKENG, JUNGERIUS, ALBERSG, LAWLEYH, DELANYI, MACEACHERNE and CHENGE2008). The inheritance of mtDNA differs from that of nuclear DNA in that it has a direct lineage to the ancestral mother. The reason for this maternal inheritance pattern is that when an egg is fertilised, the cells of the resulting embryo contain the mtDNA and cytoplasm of the egg, not of the sperm. As the embryo continues to develop all of the cells contain the cytoplasm and mtDNA of the ancestral mother. The reason for the popular adoption of mtDNA markers is that it is found in great abundance in cell cytoplasm and hence easily amplified (Galtier et al., Reference GALTIER, NABHOLZ, GLEMIN and HURST2009). Furthermore, across a wide range of animal species, the mitochondrial gene content is strongly conserved, has little duplication, has no intron, and has very short intergenic regions (Gissi et al., Reference GISSI, IANNELLI and PESOLE2008). The mtDNA also has specific biological properties, i.e. its direct link to its ancestral maternal inheritance and its involvement in metabolic functions that make it an appropriate marker of molecular biodiversity. Lastly, it is worth noting that mtDNA is of little use in investigating recent loss of genetic variation and any individual-level events such as identity, individual dispersal, and mating systems. Males will carry the mtDNA of their dam, but their offspring will carry the mtDNA of their own mother, and not of their father. Thus, only daughters will pass the mtDNA on to future generations.

Numerous published studies have reached conclusions about population history, patterns of gene flow, genetic structure, and species limits, on the basis of mtDNA sequence variation (Zink and Barrowclough, Reference ZINK and BARROWCLOUGH2008). MtDNA has been used to study phylo-geographic structure of avian species (Ceccobelli et al., Reference CECCOBELLI, DI LORENZO, LANCIONI, CASTELLINI, MONTEAGUDO IBÁÑEZ, SABBIONI, SARTI, WEIGEND and LASAGNA2013), to infer regions of domestication and to identify the number of maternal lineages and their geographic origins (FAO, 2007). The huge abundance of mtDNA makes it an excellent candidate for archaeological studies that are often old or degraded samples.

Evolution of mt-DNA studies in chicken

A large amount of research has focused on reconstructing the matrilineal history of domestic chickens using mtDNA sequence data. Chicken mtDNA sequence polymorphisms have been investigated to address the questions of maternal origin and subsequent domestication events (Silva et al., Reference SILVA, GUAN, HO-SHING, JONES, XU, HUI, NOTTER and SMITH2008). It is widely accepted that within and between populations genetic diversity is essential for effective management practices and to develop sustainable conservation strategies. Most studies of chicken mtDNA rely on sequences of partial control region (Muchadeyi et al., Reference MUCHADEYI, EDING, SIMIANER, WOLLNY, GROENEVELD and WEIGEND2008; Razafindraibe et al., Reference RAZAFINDRAIBE, MOBEGI, OMMEH, RAKOTONDRAVAO, BJØRNSTAD, HANOTTE and JIANLIN2008) but recent researches used the complete mtDNA genome to reconstruct the history of animal domestication, such as in cattle (Achilli et al., Reference ACHILLI, OLIVIERI, PELLECCHIA, UBOLDI, COLLI, AL-ZAHERY, ACCETTURO, PALA, HOOSHIAR KASHANI, PEREGO, BATTAGLIA, FORNARINO, KALAMATI, HOUSHMAND, NEGRINI, SEMINO, RICHARDS, MACAULAY, FERRETTI, BANDELT, AJMONE-MARSAN and TORRONI2008; Reference ACHILLI, BONFIGLIO, OLIVIERI, MALUSA, PALA, KASHANI, PEREGO, AJMONE-MARSAN, LIOTTA, SEMINO, BANDELT, FERRETTI and TORRONI2009; Bonfiglio et al., Reference BONFIGLIO, ACHILLI, OLIVIERI, NEGRINI, COLLI, LIOTTA, AJMONE-MARSAN, TORRONI and FERRETTI2010), pigs (Wu et al., Reference WU, YAO, QU, DING, LI, PALANICHAMY, DUAN, LI, CHEN and ZHANG2007), chicken (Miao et al., Reference MIAO, PENG, WU, OUYANG, YANG, YU, LIANG, PIANCHOU, BEJA-PEREIRA, MITRA, PALANICHAMY, BAIG, CHAUDHURI, SHEN, KONG, MURPHY, YAO and ZHANG2013) and sheep (Lancioni et al., Reference LANCIONI, DI LORENZO, CECCOBELLI, PEREGO, MIGLIO, LANDI, ANTOGNONI, SARTI, LASAGNA and ACHILLI2013). As already alluded two different hypotheses are discernible about the origin of domestic chickens. Initially, it was suggested that one sub-species of Red Junglefowl (Gallus gallus gallus) was the main progenitor of all domestic chickens and the centre of domestication event was in Southeast Asia (Fumihito et al., Reference FUMIHITO, MIYAKE, TAKADA, SHINGU, ENDO, GOJOBORI, KONDO and OHNO1996). Later on, other studies revealed that chickens have also been domesticated from multiple geographic centres of origin in South and Southeast Asia, (Kanginakudru et al., Reference KANGINAKUDRU, METTA, JAKATI and NAGARAJU2008; Oka et al., Reference OKA, INO, NOMURA, KAWASHIMA, KUWAYAMA, HANADA, AMANO, TAKADA, TAKAHATA, HAYASHI and AKISHINONOMIYA2007). Furthermore, interspecies introgressions have also occurred from the related Grey Junglefowl (Gallus sonnerati) and possibly from Ceylon Junglefowl (Gallus lafayeti) during the domestication process (Eriksson et al., Reference ERIKSSON, LARSON, GUNNARSSON, BED'HOM, TIXIER-BOICHARD, STRÖMSTEDT, WRIGHT, JUNGERIUS, VEREIJKEN, RANDI, JENSEN and ANDERSSON2008).

The first genetic study on mtDNA suggest that the Indochinese Red Junglefowl subspecies Gallus gallus gallus is the primary maternal ancestor of the domestic chicken (Gallus gallus domesticus) (Fumihito et al.,1994). Liu et al. (Reference LIU, WU, YAO, MIAO, LUIKART, BAIG, BEJA-PEREIRA, DING, GOUNDER PALANICHAMY and ZHANG2006) showed that at least three subspecies of Gallus gallus were enrolled in the origin of domestic chicken breeds, but also that there may be at least two domestication centres: one in Southeast Asia and one in the Indian subcontinent. The authors suggested nine highly divergent clades (named clade A-I) related to geographical distribution in a wide range of domestic chickens and Red Junglefowls across Eurasian regions. The study, involved 834 mtDNA sequences from domestic chickens and 66 mtDNA sequences from four Red Junglefowl subspecies (mainly Gallus gallus spadiceus, Gallus gallus gallus, Gallus gallus jabouillei and Gallus gallus bankiva), and identified a total of 169 different haplotypes clustered in nine highly divergent clades, named A to I, seven of them including both wild and domestic individuals. Clade E was the most ubiquitous, dominating in Europe, Middle East and India. Clades A and E were mainly distributed in South China and Japan; C clade was found in chickens from Japan and Southeast China, while F and G clades were only found in the northern part of Southeast China. Clade D could be associated to the distribution of game birds, used for cockfighting. Clade D was the most frequent in Red Junglefowl. Clade H was found only in Red Junglefowl and clade I was mainly present in Vietnam. Similarly, Oka et al. (Reference OKA, INO, NOMURA, KAWASHIMA, KUWAYAMA, HANADA, AMANO, TAKADA, TAKAHATA, HAYASHI and AKISHINONOMIYA2007) identified seven clades (named clade A-G) in Japanese chickens of which four clades A, B, C and E are identical to Liu's clades E, A, D and B, respectively. Additional data confirmed that domestication had occurred independently in different locations of Asia including India (Kanginakudru et al., Reference KANGINAKUDRU, METTA, JAKATI and NAGARAJU2008). A later study concluded that clade D was also the second most frequent clade in India, after clade E. Furthermore, Eriksson et al. (Reference ERIKSSON, LARSON, GUNNARSSON, BED'HOM, TIXIER-BOICHARD, STRÖMSTEDT, WRIGHT, JUNGERIUS, VEREIJKEN, RANDI, JENSEN and ANDERSSON2008) highlighted the hybrid origin of the domestic chicken, due to ancestral hybridisation involving the Grey Junglefowl (Gallus sonneratii). Three studies have made an attempt to address the origin of African village chickens through the analysis of partial mtDNA D-Loop sequences. Muchadeyi et al. (Reference MUCHADEYI, EDING, SIMIANER, WOLLNY, GROENEVELD and WEIGEND2008) observed two distinct haplogroups in Zimbabwe village chickens which they postulated came from Southeast Asia and the Indian subcontinent. Similarly, Razafindraibe et al. (Reference RAZAFINDRAIBE, MOBEGI, OMMEH, RAKOTONDRAVAO, BJØRNSTAD, HANOTTE and JIANLIN2008) observed two haplougroups in Madagascar village chicken and speculated that one was of Indonesian and the other of African continental origin or an introgression from commercial lines. At the opposite a single haplogroup thought to be of Indian origin was observed in Nigeria village chickens by Adebambo et al. (Reference ADEBAMBO, MOBEGI, MWACHARO, OLADEJO, ADEWALE, ILORI, MAKANJUOLA, AFOLAYAN, BJØRNSTAD, JIANLIN and HANOTTE2010), while no information is yet available for the East African region. Survey its genetic diversity and trace the history of domestication Miao et al. (Reference MIAO, PENG, WU, OUYANG, YANG, YU, LIANG, PIANCHOU, BEJA-PEREIRA, MITRA, PALANICHAMY, BAIG, CHAUDHURI, SHEN, KONG, MURPHY, YAO and ZHANG2013) investigated a total of 4938 mitochondrial DNA fragments including 2843 previously published and 2095 de novo units from 2044 domestic chickens and 51 Red Junglefowl (Gallus gallus). Common haplogroups A-G were shared by domestic chickens and Red Junglefowl. Rare haplougroups H-I and W-Z were specific to domestic chickens and Red Junglefowl, respectively.

The result revealed new complexities of history in chicken's domestication because the phylogeny lineages from the Red Junglefowl were mingled with those of the domestic chickens.

Conclusions

In conclusion, mtDNA studies provide a valuable preliminary description of the population structure and demographic history, but nuclear markers (such as microsatellite and SNPs) would provide valuable additional information to complete the analysis. Several mtDNA studies demonstrated that domestic chicken is closely related to Red Junglefowl, although genetic contributions from other Junglefowls is evident. Furthermore, the chicken mitochondrial genome provides an opportunity to study their human-mediated dispersal out of domestication centres. Future archaeological investigations and multidisciplinary research, including genetic studies, are required to unravel more details.

Acknowledgments

The authors wish to thank the referee for the valuable comments to the manuscript and the constructive suggestions.

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