A slow march along the South American Dry Diagonal: a multi-gene molecular phylogeny and biogeographical history of the peanut genus, Arachis L.

Background and aims: Arachis contains 84 accepted species, including peanut (Arachis hypogaea), all endemic to South America. To better understand evolutionary patterns in Arachis, we studied its phylogeny and biogeographical history.

Methods: We sequenced ITS, ETS, psbA-trnH, rpoB-trnCGCA and ycf1 regions and constructed maximum likelihood trees based on aligned matrices and on a concatenation of all five regions. We then conducted a fossil-calibrated Bayesian phylogenetic analysis and a biogeographical analysis.

Key results: We hypothesize that Arachis diverged from its sister Stylosanthes in the Middle Miocene, about 15 Ma, in the area now occupied by the Brazilian Caatinga and Northeastern Cerrado, accompanied by the innovation of geocarpy as a possible adaptation to increasing aridity. Arachis began to diversify about 10 Ma, and the deepest branching, and more species-poor lineages remain associated with the Caatinga. Expansion of two distinct lineages to the contiguous and nascent Cerrado occurred in the late Miocene by ∼7.4 and ∼5.5 Ma, respectively. The Cerrado remains the major centre of diversity of Arachis and is the area of progressive expansion of the genus along the broad corridor of the north-eastern-south-western Neotropical Dry Diagonal, during the late Miocene and Pliocene. Further Pliocene expansion of distinct Arachis lineages from the Cerrado to the Pantanal and Chaco regions are also hypothesized, where the latter two ecoregions are identified as secondary centres of diversification of the genus. Frequent diversifications occurred in section Arachis from the Middle Pleistocene (∼0.774 Ma), probably driven by climate change, and accompanied by expansion of distinct Cerrado lineages: two into the Chaco, comprising a subclade of A genome species and another of all K-genome species, and a third comprising a subset of B genome species into the Chiquitano.

Conclusions: Our results clarify phylogenetic relationships in Arachis and provide a new framework to understand its evolutionary history.