Genome Analysis Traces Regional Dispersal of Rice in Taiwan and Southeast Asia
Ornob AlamRafał M. GutakerCheng‐Chieh WuKaren A. HicksR. Kyle BocinskyCristina CastilloStephen AcabadoDorian Q. FullerJade d’Alpoim GuedesYue‐Ie HsingMichael D. Purugganan
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Abstract:
The dispersal of rice (Oryza sativa) following domestication influenced massive social and cultural changes across South, East, and Southeast (SE) Asia. The history of dispersal across islands of SE Asia, and the role of Taiwan and the Austronesian expansion in this process remain largely unresolved. Here, we reconstructed the routes of dispersal of O. sativa ssp. japonica rice to Taiwan and the northern Philippines using whole-genome resequencing of indigenous rice landraces coupled with archaeological and paleoclimate data. Our results indicate that japonica rice found in the northern Philippines diverged from Indonesian landraces as early as 3,500 years before present (BP). In contrast, rice cultivated by the indigenous peoples of the Taiwanese mountains has complex origins. It comprises two distinct populations, each best explained as a result of admixture between temperate japonica that presumably came from northeast Asia, and tropical japonica from the northern Philippines and mainland SE Asia, respectively. We find that the temperate japonica component of these indigenous Taiwan populations diverged from northeast Asia subpopulations at about 2,600 BP, whereas gene flow from the northern Philippines had begun before ∼1,300 BP. This coincides with a period of intensified trade established across the South China Sea. Finally, we find evidence for positive selection acting on distinct genomic regions in different rice subpopulations, indicating local adaptation associated with the spread of japonica rice.Keywords:
Mainland
Phytolith
Archaeobotanical information relating to early plant cultivation and domestication and derived from microfossil research is rapidly expanding. In this paper I review recent data, focusing on the lowland tropics of Central and South America and primarily on phytolith, starch grain, and where available, ancient DNA remains. New and important macrobotanical evidence is also discussed. I more briefly review recent developments in other regions of the Americas and the Old World, in order to provide a broader survey of microfossil contributions to early agriculture studies. Data generated during the past ten years impact old and newer debates concerning how and when important crop plants arose and spread, and when effective food production – defined as systemic cultivation that supplied stable and significant dietary inputs – began. Phytolith and starch grain applications provide information at various, fundamental levels of understanding ranging from basic identifications of wild and domesticated species, to the direct documentation of ancient diets through recovery from the calculus of human teeth, to the generation of data on the evolution of domestication genes in some major crops.
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Paleoethnobotany
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Gene flow plays an important role in domestication history of domesticated species. However, little is known about the demographic history of domesticated silkworm involving gene flow with its wild relative.In this study, four model-based evolutionary scenarios to describe the demographic history of B. mori were hypothesized. Using Approximate Bayesian Computation method and DNA sequence data from 29 nuclear loci, we found that the gene flow at bottleneck model is the most likely scenario for silkworm domestication. The starting time of silkworm domestication was estimated to be approximate 7,500 years ago; the time of domestication termination was 3,984 years ago. Using coalescent simulation analysis, we also found that bi-directional gene flow occurred during silkworm domestication.Estimates of silkworm domestication time are nearly consistent with the archeological evidence and our previous results. Importantly, we found that the bi-directional gene flow might occur during silkworm domestication. Our findings add a dimension to highlight the important role of gene flow in domestication of crops and animals.
Coalescent theory
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Results from studies on the domestication process of Asian rice Oryza sativa have been controversial because of its complicated evolutionary history. Previous studies have yielded two alternative hypotheses about the origin(s) of the two major groups of O. sativa: japonica and indica. One study proposes a single common wild ancestor, whereas the other suggests that there were multiple domestication events of different types of wild rice. Here, we provide clear evidence of the independent domestication of japonica and indica obtained via high-throughput sequencing and a large-scale comparative analysis of two wild rice accessions (W1943 and W0106) and two cultivars (a japonica cultivar called "Nipponbare" and an indica cultivar called "Guangluai-4"). The different domestication processes of the two cultivar groups appear to have led to distinct patterns of molecular evolution in protein-coding regions. The intensity of purifying selection was relaxed only in the japonica group, possibly because of a bottleneck effect. Moreover, a genome-wide comparison between Nipponbare, Guangluai-4, and another indica cultivar (93-11) suggests multiple hybridization events between japonica and indica, both before and after the divergence of the indica cultivars. We found that a large amount of genomic DNA, including domestication-related genes, was transferred from japonica to indica, which might have been important in the development of modern rice. Our study provides an overview of the dynamic process of Asian rice domestication, including independent domestication events and subsequent gene flow.
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Gene pool
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ABSTRACT The role of gene flow in autogamous domesticated species diversity and their wild relatives is an issue that requires more field data. Using nine microsatellite loci, an analysis was done of the magnitude and direction of gene flow in the wild–weedy–domesticated complex of Phaseolus lunatus L. under traditional agricultural conditions in four regions on the Yucatan Peninsula, Mexico, its center of domestication and diversity in Mesoamerica. Two complementary methods were used. The Bayesian genotype assignment approach showed that recent gene flow was low at both the intraregional and interregional levels. The same was found with the frequency method for long‐term gene flow ( Nm intraregional from 0.31 to 0.51, and Nm interregional = 0.44). In addition, the gene flow from domesticate to wild populations was three times higher than in the opposite direction. This asymmetry can be explained by regional agricultural practices and seed selection criteria. Domesticate alleles were shown to be entering wild populations of different agricultural regions, suggesting exchange of domesticated seed between farmers of different regions. These results are very important because they show that P. lunatus on the Yucatan Peninsula has a predominantly domesticate to wild gene flow. This situation may lead to genetic assimilation of wild lima bean by its domesticated counterpart and may lead to the possible escape of transgenes in this center of origin and diversity.
Introgression
Gene pool
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Bulliform phytoliths play an important role in researching rice origins as they can be used to distinguish between wild and domesticated rice. Rice bulliform phytoliths are characterized by numerous small shallow fish-scale decorations on the lateral side. Previous studies have shown that domesticated rice has a larger number of these decorations than wild rice and that the number of decorations ≥9 is a useful feature for identifying domesticated rice. However, this standard was established based on limited samples of modern rice plants. In this study, we analyzed soil samples from both wild and domesticated rice paddies. Results showed that, in wild rice soil samples, the proportion of bulliform phytoliths with ≥9 decorations was 17.46% ± 8.29%, while in domesticated rice soil samples, the corresponding proportion was 63.70% ± 9.22%. This suggests that the proportion of phytoliths with ≥9 decorations can be adopted as a criterion for discriminating between wild and domesticated rice in prehistoric soil. This indicator will be of significance in improving the application of fish-scale decorations to research into rice origins and the rice domestication process.
Phytolith
Oryza rufipogon
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The domestication history of rice remains controversial, with multiple studies reaching different conclusions regarding its origin(s). These studies have generally assumed that populations of living wild rice, O. rufipogon , are descendants of the ancestral population that gave rise to domesticated rice, but relatively little attention has been paid to the origins and history of wild rice itself. Here, we investigate the genetic ancestry of wild rice by analyzing a diverse panel of rice genomes consisting of 203 domesticated and 435 wild rice accessions. We show that most modern wild rice is heavily admixed with domesticated rice through both pollen- and seed-mediated gene flow. In fact, much presumed wild rice may simply represent different stages of feralized domesticated rice. In line with this hypothesis, many presumed wild rice varieties show remnants of the effects of selective sweeps in previously identified domestication genes, as well as evidence of recent selection in flowering genes possibly associated with the feralization process. Furthermore, there is a distinct geographical pattern of gene flow from aus , indica , and japonica varieties into colocated wild rice. We also show that admixture from aus and indica is more recent than gene flow from japonica , possibly consistent with an earlier spread of japonica varieties. We argue that wild rice populations should be considered a hybrid swarm, connected to domesticated rice by continuous and extensive gene flow.
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Weedy rice
Gene pool
Introgression
Oryza
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Significance When the domestication of rice began in its homeland, China, is an enduring and important issue of debate for researchers from many different disciplines. Reliable chronological and robust identification criteria for rice domestication are keys to understanding the issue. Here, we first use phytolith dating to constrain the initial occupation of Shangshan, an important site with early rice remains located in the Lower Yangtze region of China. We then identify the rice phytoliths of Shangshan as partly domesticated based on their morphological characteristics. The results indicate that rice domestication may have begun at Shangshan in the Lower Yangtze during the beginning of the Holocene.
Phytolith
Homeland
Yangtze river
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Phytolith
Glume
Cuneiform
Yangtze river
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Crop domestication and the subsequent expansion of crops have long been thought of as a linear process from a wild ancestor to a domesticate. However, evidence of gene flow from locally adapted wild relatives that provided adaptive alleles into crops has been identified in multiple species. Yet, little is known about the evolutionary consequences of gene flow during domestication and the interaction of gene flow and genetic load in crop populations. We study the pseudo-cereal grain amaranth that has been domesticated three times in different geographic regions of the Americas. We quantify the amount and distribution of gene flow and genetic load along the genome of the three grain amaranth species and their two wild relatives. Our results show ample gene flow between crop species and between crops and their wild relatives. Gene flow from wild relatives decreased genetic load in the three crop species. This suggests that wild relatives could provide evolutionary rescue by replacing deleterious alleles in crops. We assess experimental hybrids between the three crop species and found genetic incompatibilities between one Central American grain amaranth and the other two crop species. These incompatibilities might have created recent reproductive barriers and maintained species integrity today. Together, our results show that gene flow played an important role in the domestication and expansion of grain amaranth, despite genetic species barriers. The domestication of plants was likely not linear and created a genomic mosaic by multiple contributors with varying fitness effects for today’s crops.
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