A population genomics appraisal suggests independent dispersals for bitter and sweet manioc in Brazilian Amazonia

Abstract

Amazonia is a major world centre of plant domestication, but the genetics of domestication remains unclear for most Amazonian crops. Manioc (Manihot esculenta) is the most important staple food crop that originated in this region. Although manioc is relatively well-studied, little is known about the diversification of bitter and sweet landraces and how they were dispersed across Amazonia. We evaluated single nucleotide polymorphisms (SNPs) in wild and cultivated manioc to identify outlier SNPs putatively under selection and to assess the neutral genetic structure of landraces to make inferences about the evolution of the crop in Amazonia. Some outlier SNPs were in putative manioc genes possibly related to plant architecture, transcriptional regulation and responses to stress. The neutral SNPs revealed contrasting genetic structuring for bitter and sweet landraces. The outlier SNPs may be signatures of the genomic changes resulting from domestication, while the neutral genetic structure suggests independent dispersals for sweet and bitter manioc, possibly related to the earlier domestication and diversification of the former. Our results highlight the role of ancient peoples and current smallholders in the management and conservation of manioc genetic diversity, including putative genes and specific genetic resources with adaptive potential in the context of climate change.

Selective signatures and high genome-wide diversity in traditional Brazilian manioc (Manihot esculentaCrantz) varieties

“…This result may also reflect many founding events (Allaby et al 2019) that accompanied the rapid spread of the crop across the Neotropics (Isendahl 2011) and the wide dispersal across the world. The observed genetic divergence was similar to our previous study (Alves-Pereira et al 2020), but more geographically extensive sampling of wild populations would improve our understanding about the current population dynamics between wild and cultivated manioc. Recent genomic approaches evidenced introgressions from some wild relatives in the genome of cultivated manioc (Bredeson et al 2016;Wolfe et al 2019).…”

“…Although the groups of manioc varieties are not true populations, some aspects, such as the possibility of crossings and incorporation of sexual plants into clonally propagated varieties, make these groups biologically meaningful. Moreover, genetic approaches provided interesting results even when using generic groups of manioc varieties (Bradbury et al 2013;Alves-Pereira et al 2020) and limited sample sizes in other study systems (Talavera et al 2019;Kates et al 2021). The selective signatures discussed above should be regarded as initial hypotheses and further genome-wide association studies and quantitative trait loci mapping are required to confirm their biological significance (Barrett and Hoekstra 2011;Meyer and Purugganan 2013).…”

“…The influence of ecogeographic variation in the distribution of genetic diversity in manioc is variable (Siqueira et al 2009;Mühlen et al 2019;Ogbonna et al 2021a), but the existence of divergent varieties from different biomes may also reflect the selection under distinct ecological and cultural contexts. Nonetheless, the genetic divergence between bitter and sweet manioc seems to be higher in Amazonia than outside this region (Bradbury et al 2013;Alves-Pereira et al 2020). It is possible that divergent selective pressures for bitterness or sweetness are more relaxed outside Amazonia, because the crop's dispersals were not always accompanied by cultural appropriation (McKey and Delêtre 2017).…”

“…These varieties were originally collected in smallholder farmer communities in six Brazilian states, located in four different biomes: Amazonia (16), Cerrado (30), Atlantic Forest (27) and Pantanal (5) (Figure 1, Table S1). We also evaluated other samples collected in a previous study (Alves-Pereira et al 2020): eight M. esculenta ssp. flabellifolia samples collected in the center of manioc domestication in Rondônia state, and six Amazonian varieties (three bitter and three sweet).…”

Green, yellow or black? Genetic differentiation and adaptation signatures in a highly migratory marine turtle

“…Although several tests for the identification of outlier loci have been developed, they may not account for population structure and its covariance with other variables (such as demography and mutation rates) accurately, which could lead to false positives [39]. To resolve this issue, three methods based on different models were run in the software BayeScan, Fsthet and PCAdapt.…”