Potential dual expansion of domesticated donkeys revealed by worldwide analysis on mitochondrial sequences.

Xiyao Ma ,Chen Xi,Olaogun Sunday Charles,Abdulloevich Najmudinov Tojiddin,Adeola Adeniyi C,Wu Shi-Fang,Liu He-Qun,Afanasevna Manilova Elena,Li Jie,Isakova Jainagul,Ibrohimovich Khudoidodov Behruz,Esmailizadeh Ali,Wang Zhe,Bernard Agwanda ,Sheila Ommeh ,Jacqueline Kasiiti Lichoti ,Min‐Sheng Peng ,Tangyuan Ning ,Godwin F Mangbon ,Almaz Aldashev ,R A M Adedokun ,Oscar J Sanke ,Weikang Yang ,Yán Li ,Yaping Zhang

doi:10.24272/j.issn.2095-8137.2020.007

Abstract

Molecular studies on donkey mitochondrial sequences have clearly defined two distinct maternal lineages involved in domestication. However, domestication histories of these two lineages remain enigmatic. We therefore compared several population characteristics between these two lineages based on global sampling, which included 171 sequences obtained in this study (including Middle Asian, East Asian, and African samples) plus 536 published sequences (including European, Asian, and African samples). The two lineages were clearly separated from each other based on whole mitochondrial genomes and partial non-coding displacement loop (D-loop) sequences, respectively. The Clade I lineage experienced an increase in population size more than 8 000 years ago and shows a complex haplotype network. In contrast, the population size of the Clade II lineage has remained relatively constant, with a simpler haplotype network. Although the distribution of the two lineages was almost equal across the Eurasian mainland, they still presented discernible but complex geographic bias in most parts of Africa, which are known as their domestication sites. Donkeys from sub-Saharan Africa tended to descend from the Clade I lineage, whereas the Clade II lineage was dominant along the East and North coasts of Africa. Furthermore, the migration routes inferred from diversity decay suggested different expansion across China between the two lineages. Altogether, these differences indicated non-simultaneous domestication of the two lineages, which was possibly influenced by the response of pastoralists to the desertification of the Sahara and by the social expansion and trade of ancient humans in Northeast Africa, respectively.

Highlights

Unlike other species with a similar historical function, domestic donkeys are underrepresented in the scientific literature (Blench, 2000)
We constructed a highly supported phylogenetic tree based on the 77 mitochondrial DNA (mtDNA) genome sequences from the current study combined with seven mtDNA genomes downloaded from National Center for Biotechnology Information (NCBI) (Supplementary Table S1)
Using the horse as an outgroup, the Somali wild ass formed a sister clade with all donkeys, a topology highly differentiated from that based on displacement loop (D-loop) sequences, which was highly supported by the neighbor-joining, maximum likelihood, and Bayesian methods analyzed here (Figure 1)

Summary

Introduction

Unlike other species with a similar historical function (e.g., horses), domestic donkeys are underrepresented in the scientific literature (Blench, 2000). Donkeys remain an essential means of transport in modern society for people living in mountain areas, deserts, and poorer regions of the world (Smith & Pearson, 2005; Starkey, 2000) Both molecular data and archaeological evidence strongly support an African origin for the domestic donkey (Equus asinus) (Beja-Pereira et al, 2004; Kimura et al, 2011; Rossel et al, 2008). Ancient DNA illustrates the extensive distribution of the Nubian and Somali wild ass in Northeast Africa (Kimura et al, 2011), alluding to potential geographic overlaps between the Nubian wild ass and ancestors of the Clade II donkeys As such, whether these two distinct lineages were domesticated simultaneously or not remains controversial, even though they probably originated from two mitochondrially distinct wild asses (Jordana et al, 2016; Xia et al, 2019)

Methods

Results

Conclusion