Evolutionary Processes Involved in the Emergence and Expansion of an Atypical O. sativa Group in Madagascar

Understanding crops genetic diversity and the evolutionary processes that accompanied their worldwide spread is useful for designing effective breeding strategies. Madagascar Island was one of the last major Old World areas where human settlement brought the introduction of Oryza sativa. Early studies in the island had reported the presence of a rice group specific to Madagascar. Using 24 K SNP, we compared diversity patterns at the whole genome and at haplotype (30 SNP-long segments along the genome) levels, between 620 Malagasy and 1929 Asian rice accessions. The haplotype level analysis aimed at identifying local genotypic variations, relative to the whole genome level, using a group assignment method that relies on kernel density estimation in a Principal Component Analysis feature space. Migration bottleneck had resulted in 10–25% reduction of diversity among the Malagasy representatives of indica and japonica populations. Compared to their Asian counterpart, they showed slightly lower indica and japonica introgressions, suggesting the two populations had undergone less recombination when migration to the island occurred. The origins of the Malagasy indica and japonica groups were delineated to indica subpopulation from the Indian subcontinent and to tropical japonica from the Malay Archipelago, respectively. The Malagasy-specific group (Gm) had a rather high gene diversity and an original haplotype pattern: much lower share of indica haplotypes, and much higher share of Aus and japonica haplotypes than indica. Its emergence and expansion are most probably due to inter-group recombination facilitated by sympatry between indica-Aus admixes and “Bulu” type landraces of japonica in the central high plateaux of Madagascar, and to human selection for adaptation to the lowland rice cultivation. Pattern of rice genetic diversity was also tightly associated with the history of human settlement in the island. Emergence of the Gm group is associated with the latest arrivals of Austronesians, who founded the Merina kingdom in the high plateaux and developed lowland rice cultivation. As an intermediary form between Aus, indica and japonica, the three pillars of O. sativa domestication, Gm represents a very valuable genetic resource in breeding for adaptation to cold tolerance in tropical highlands. We proposed the name Rojo for this new rice group. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-021-00479-8.