Domestication, hybridization, speciation, and the origins of an economically important tree crop of Spondias (Anacardiaceae) from the Brazilian Caatinga dry forest

Abstract

Domestication can be defined as evolution driven by artificial selection by humans, where individuals possessing desirable characteristics are favored and selectively propagated; over time this process leads to morphological, physiological and genetic changes that distinguish domesticated taxa from their wild ancestors, many times to the point in that the domesticated taxon is regarded as a distinct species. In this paper we address plants of Spondias known by the vernacular name umbu­caja in Northeast Brazil. These plants are found in managed landscapes, but natural populations have not been identified due to widespread cultivation coupled with the clearing of original vegetation. Umbu­caja can be regarded as domesticated because it appears to occur exclusively in cultivation, being actively maintained and propagated by man due to its juicy, delicious fruits. Umbu­caja is referred to as being of hybrid origin in the literature, but this hypothesis remains largely untested experimentally. We carried out a thorough comparative examination of the overall morphology and also a morphometric analysis of leaf and fruit characters of populations of umbu­caja and other Spondias species found in Northeast Brazil. We also reconstructed phylogenies and haplotype networks based on sequences of two non­coding cpDNA regions and the nuclear ETS region in order to ascertain the genetic affinities of umbu­caja. Additionally we estimated the ages of diversification events in Spondias in order to determine when umbu­caja diverged from related species. Although displaying some morphometric intermediacy in the leaves, a number of morphological features readily distinguish umbu­caja from its nearest relatives Spondias tuberosa and S. venulosa. No haplotypes were found to be shared between distinct Spondias species, except in the ETS dataset where umbu­caja and S. tuberosa shared the same haplotype. In the cpDNA dataset, haplotypes of umbu­caja are nearest to haplotypes of S. venulosa, but genetic distances within each taxon are smaller than the genetic distance between the two taxa, suggesting different gene pools for each taxon. There is incongruence in the placement of umbu­caja haplotypes in the cpDNA versus ETS datasets, and also incongruence in the trees recovered from the phylogenetic analyses of both datasets, which is an indication that umbu­caja might have a hybrid origin with S. venulosa and S. tuberosa as its parents. However, umbu­caja was found to have diverged from S. venulosa 3.79 million years ago, indicating that this taxon originated from natural processes. Based on the results of the molecular, morphometric, morphological and time divergence investigations we conclude that umbu­caja should be regarded as distinct lineage that remained undescribed because at present it seems to be only known from cultivation, and also due to its putative hybrid origin. We therefore describe this taxon as Spondias bahiensis sp. nov.