Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Apr 4;12(4):jkac029.
doi: 10.1093/g3journal/jkac029.

The genetic history of Mayotte and Madagascar cattle breeds mirrors the complex pattern of human exchanges in Western Indian Ocean

Jessica Magnier  1   2 , Tom Druet  3 , Michel Naves  4 , Mélissa Ouvrard  5 , Solène Raoul  5 , Jérôme Janelle  1   6 , Katayoun Moazami-Goudarzi  7 , Matthieu Lesnoff  1   2 , Emmanuel Tillard  1   6 , Mathieu Gautier  8 , Laurence Flori  9
Affiliations

The genetic history of Mayotte and Madagascar cattle breeds mirrors the complex pattern of human exchanges in Western Indian Ocean

Jessica Magnier et al. G3 (Bethesda). .

Abstract

Despite their central economic and cultural role, the origin of cattle populations living in Indian Ocean islands still remains poorly documented. Here, we unravel the demographic and adaptive histories of the extant Zebus from the Mayotte and Madagascar islands using high-density SNP genotyping data. We found that these populations are very closely related and both display a predominant indicine ancestry. They diverged in the 16th century at the arrival of European people who transformed the trade network in the area. Their common ancestral cattle population originates from an admixture between an admixed African zebu population and an Indian zebu that occurred around the 12th century at the time of the earliest contacts between human African populations of the Swahili corridor and Austronesian people from Southeast Asia in Comoros and Madagascar. A steep increase in the estimated population sizes from the beginning of the 16th to the 17th century coincides with the expansion of the cattle trade. By carrying out genome scans for recent selection in the two cattle populations from Mayotte and Madagascar, we identified sets of candidate genes involved in biological functions (cancer, skin structure, and UV-protection, nervous system and behavior, organ development, metabolism, and immune response) broadly representative of the physiological adaptation to tropical conditions. Overall, the origin of the cattle populations from Western Indian Ocean islands mirrors the complex history of human migrations and trade in this area.

Keywords: Indian Ocean; adaptation; cattle; demography; genomics.

PubMed Disclaimer

Figures

Fig. 1.
Fig. 1.
Results of the PCA and unsupervised hierarchical clustering including HD genotyping data (528 individuals from 13 populations genotyped for 680,338 SNPs). a) PCA results. The individuals are plotted on the first two principal components according to their coordinates. Ellipses characterize the dispersion of each population around its center of gravity. MAY and ZMA individuals are plotted in dark-pink and pink and EAZ and ZFU individuals in purple and dark purple, respectively. EUT, AFT, and ZEB individuals are plotted in blue, green, and red, respectively. b) Unsupervised hierarchical clustering results with K = 3 predefined clusters. For each individual, the proportions of each cluster (y-axis) which were interpreted as representative of EUT, AFT, and ZEB ancestries are plotted in blue, green, and red, respectively.
Fig. 2.
Fig. 2.
Inferred admixture graph connecting cattle breeds from Mayotte and Madagascar (MAY and ZMA, in yellow) with two Indian indicine breeds (GIR and NEL in red), one African zebu breed (EAZ in purple), two AFT breeds (LAG and NDA in green) and one European taurine breed (HOL in blue). Admixture events are shown by dotted arrows. Estimates of branch lengths (×103, in drift units of t2Ne) and admixture rates are indicated next to the corresponding edges. The Z-score of the worst fitted f-statistics f4(MAY, ZMA; HOL, LAG) is equal to –1.04.
Fig. 3.
Fig. 3.
Population size history (Ne) of MAY and ZMA populations estimated with GONE (Santiago et al. 2020). The average Ne trajectories (dashed line) and 95% confidence envelope estimated from block-jackknife samples are plotted in green for ZMA and red for MAY. The time scale was transformed into calendar assuming a 6-year generation time for cattle and accounting for the difference in sampling time between ZMA (1990) and MAY (2016). The estimated timing of the admixture event (tαioz) that led to the common hybrid ancestor (named Indian Ocean Zebus in the main text) of MAY and ZMA is given in orange. The orange asterisk gives the likely splitting time (beginning of the 16th century, i.e., tS≃80 generations before MAY sampling time) between MAY and ZMA roughly estimated from the separation of the two trajectories.
Fig. 4.
Fig. 4.
Characterization of individual inbreeding levels in Mayotte and Madagascar breeds. a) Violin plots representing the distribution of inbreeding coefficients for the MAY (N = 30) and ZMA (N = 23) breeds, colored in pink and purple, respectively. b) Partitioning of individual genomes in different HBD classes. Each bar represents an individual and its total height the overall level of inbreeding. The height of the different stacks, which appear in different colors, represents the proportion of the genome associated with each HBD class, defined by their rate Rk. c) Average proportion of individual genomes associated with different HBD classes for MAY (pink) and ZMA (purple) populations. Individual proportions of the genome associated with a specific HBD class are obtained by averaging the corresponding HBD-classes probabilities over all marker positions.
Fig. 5.
Fig. 5.
Gene networks including candidate genes under selection detected in at least one iHS or Rsb test in the genome of breeds from Mayotte (a) and Madagascar (b)
See this image and copyright information in PMC

References

    1. Alexander DH, Novembre J, Lange K.. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655–1664. - PMC - PubMed
    1. Bahbahani H, Clifford H, Wragg D, Mbole-Kariuki MN, Tassell CV, Sonstegard T, Woolhouse M, Hanotte O.. Signatures of positive selection in East African Shorthorn Zebu: a genome-wide single nucleotide polymorphism analysis. Sci Rep. 2015;5(1):11729. - PMC - PubMed
    1. Bahbahani H, Tijjani A, Mukasa C, Wragg D, Almathen F, Nash O, Akpa GN, Mbole-Kariuki M, Malla S, Woolhouse M, et al. Signatures of selection for environmental adaptation and Zebu x Taurine hybrid fitness in East African Shorthorn Zebu. Front Genet. 2017;8:68. - PMC - PubMed
    1. Beaujard P. The Indian Ocean in Eurasian and African world-systems before the sixteenth century. J World Hist. 2005;16(4):411.
    1. Beaujard P. East Africa, the Comoros Islands and Madagascar before the sixteenth century: on a neglected part of the world system. Azania Archaeol Res Africa. 2007;42(1):15–35.