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DNA markers reveal the complexity of livestock domestication

Key Points

  • The origins of domestic livestock have long been controversial and have presented a powerful challenge to archeozoologists. Molecular analysis is now helping to unravel when and where livestock domestication occurred.

  • The use of mitochondrial DNA sequencing has revealed a surprisingly complex history of domestication, with numerous mitochondrial lineages being the rule in sequences from the DNA of modern and ancient livestock samples.

  • One pattern that emerges in several species (cattle, sheep and pigs, for example) is that they are the result of apparently independent domestication events in the Middle/Near east and east Asia. Africa also seems to have been an important region for cattle domestication.

  • Other molecular markers, such as microsatellites, can give more insight into the recent demographic history of domestic breeds, such as the effects of population bottlenecks, selection, genetic drift and inbreeding, and introgression. The influence of these different demographic events is extremely strong in some breeds.

  • Modern-day patterns of genetic diversity in livestock therefore only partially reflect this complex origin, owing to subsequent translocations by humans and the effects of introgression between different DNA lineages. This makes interpreting the genetic diversity in modern livestock extremely challenging.

  • Conservation of livestock diversity must account for the complex histories of the livestock breeds now under threat of extinction across the globe. A range of molecular markers, especially including those that reflect their evolution, recent demographics and economic potential should be applied in combination to provide optimal data for livestock management and conservation.

Abstract

A series of recent genetic studies has revealed the remarkably complex picture of domestication in both New World and Old World livestock. By comparing mitochondrial and nuclear DNA sequences of modern breeds with their potential wild and domestic ancestors, we have gained new insights into the timing and location of domestication events that produced the farm animals of today. The real surprise has been the high number of domestication events and the diverse locations in which they took place — factors which could radically change our approach to conserving livestock biodiversity resources in the future.

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Figure 1: The principal centres of animal domestication.
Figure 2: Phylogenetic complexity in modern-day cattle and horses.
Figure 3: Phylogenetic complexity in modern-day sheep and goats.
Figure 4: Cattle and goat mitochondrial diversity in Eurasia.

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Acknowledgements

M.W.B. would like to acknowledge funding from the UK Ministry of Agriculture, Fisheries and Food and the European Commission (ECONOGENE project). S. Townsend, K. Byrne, L. Chikhi, G.M. Hewitt, L. Alderson, The Rare Breeds Survival Trust, J. Wheeler, R, Rosadio, M. Kadwell and M. Fernandez have all contributed significantly to M.W.B.'s livestock research. G.L. was supported by grants from NATO, the German Federal Agency for Nature Conservation (Scientific Authority to CITES), the French CNRS/INSERM sequencing programme and the European Commission (ECONOGENE project).

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Correspondence to Michael W. Bruford.

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FURTHER INFORMATION

Food and Agriculture Organization of the United Nations

2002 IUCN Red List of Threatened Species

Glossary

DOMESTICATION

The process of genetically adapting an animal or plant to better suit the needs of human beings (for example, breeding cattle for milk production).

ANTHROPOLOGY

The study of humans and non-human primates, which includes the comparative study of societies and cultures and the science of human zoology and evolution.

ARCHAEOBIOLOGY

The study of non-human animal, plant and microbial remains in archaeological sites.

ANIMAL GENETIC RESOURCES

(AnGR). Genetic diversity, either characterized or as yet uncharacterized, that is found in economically important animals, plants and microbes. This does not indicate that these species are necessarily domesticated.

CAMELID

A mammal of the Camelidae family comprising camels, the llama and its relatives (for example, the alpaca).

ARCHAEOZOOLOGY

The study of non-human animal remains in archaeological sites.

FERTILE CRESCENT

A region that spans modern-day Israel, Jordan, Lebanon and western Syria, into southeast Turkey and, along the Tigris and Euphrates rivers, into Iraq and the western flanks of Iran.

HAPLOTYPES

Genetic loci which co-segregate or are in linkage disequilibrium (LD). As mitochondrial DNA is a small extranuclear molecule, which does not undergo recombination, all markers on this genome are effectively linked as a single haplotype. At present, LD mapping is being used effectively in several species, including humans and livestock, to identify regions of the nuclear genome that have undergone intense episodes of selection.

MOLECULAR CLOCK

The principle that any gene or protein has a near-constant long-term rate of evolution in all branches of a clade, which means that the amount of sequence divergence between two sequences will be proportional to the amount of time elapsed since their shared ancestor existed.

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM

(AFLP). PCR-linker-generated multifragment profiles (DNA fingerprints) that are predominantly inherited in a dominant fashion, but that have recently proved useful as tools for genetic diversity estimation and in genome mapping projects.

BOTTLENECKS

Episodes of demographic contraction (small population size) that might result in reduced genetic variation and loss of viability of populations in future generations in the absence of immigration of new genetic material.

PARSIMONY

As applied to phylogenetic reconstruction, a criterion for estimating historical changes by minimizing the number of substitution events that are required to explain how one DNA sequence evolves into another.

RESTRICTION FRAGMENT LENGTH POLYMORPHISM

(RFLP). A fragment length variant in DNA sequences that is generated through the gain or loss of a restriction site owing to a DNA substitution.

MAXIMUM-LIKELIHOOD

A method that selects the phylogenetic tree that has the highest probability of explaining the sequence data, under a specific model of substitution (changes in the nucleotide or amino-acid sequence).

NEIGHBOUR-JOINING

A distance-based molecular phylogenetic method that involves the sequential addition of taxa and the minimization of branch lengths, but does not assume a molecular clock.

BOOTSTRAP ANALYSIS

A type of statistical analysis to test the reliability of certain branches in an evolutionary tree. The bootstrap proceeds by re-sampling the original data, with replacement, to create a series of bootstrap samples of the same size as the original data. The bootstrap value of a node is the percentage of times that a node is present in the set of trees that is constructed from the new data sets.

COALESCENCE

The joining of genetic lineages to common ancestors when they are traced backwards in time.

INTROGRESSION

The transfer or genetic material from one species to another by hybridization and repeated backcrossing.

EVOLUTIONARILY SIGNIFICANT UNIT

Populations that share a common ancestor, but that have been demographically independent for long enough that they no longer share mitochondrial DNA haplotypes.

MANAGEMENT UNIT

Populations that have significant allele or haplotype frequency differences at mitochondrial DNA and nuclear DNA.

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Bruford, M., Bradley, D. & Luikart, G. DNA markers reveal the complexity of livestock domestication. Nat Rev Genet 4, 900–910 (2003). https://doi.org/10.1038/nrg1203

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