The history of sweet potato in the Pacific has long been an enigma. Archaeological, linguistic, and ethnobotanical data suggest that prehistoric human-mediated dispersal events contributed to the distribution in Oceania of this American domesticate. According to the "tripartite hypothesis," sweet potato was introduced into Oceania from South America in pre-Columbian times and was then later newly introduced, and diffused widely across the Pacific, by Europeans via two historically documented routes from Mexico and the Caribbean. Although sweet potato is the most convincing example of putative pre-Columbian connections between human occupants of Polynesia and South America, the search for genetic evidence of pre-Columbian dispersal of sweet potato into Oceania has been inconclusive. Our study attempts to fill this gap. Using complementary sets of markers (chloroplast and nuclear microsatellites) and both modern and herbarium samples, we test the tripartite hypothesis. Our results provide strong support for prehistoric transfer(s) of sweet potato from South America (Peru-Ecuador region) into Polynesia. Our results also document a temporal shift in the pattern of distribution of genetic variation in sweet potato in Oceania. Later reintroductions, accompanied by recombination between distinct sweet potato gene pools, have reshuffled the crop's initial genetic base, obscuring primary patterns of diffusion and, at the same time, giving rise to an impressive number of local variants. Moreover, our study shows that phenotypes, names, and neutral genes do not necessarily share completely parallel evolutionary histories. Multidisciplinary approaches, thus, appear necessary for accurate reconstruction of the intertwined histories of plants and humans.phylogeography | herbarium specimens | prehistory | early trans-Pacific travels
Behaviour and genetic structure are intimately related: mating patterns and patterns of movement between groups or populations influence the movement of genetic variation across the landscape and from one generation to the next. In hybrid zones, the behaviour of the hybridizing taxa can also impact the incidence and outcome of hybridization events. Hybridization between yellow baboons and anubis baboons has been well documented in the Amboseli basin of Kenya, where more anubis-like individuals tend to experience maturational and reproductive advantages. However, it is unknown whether these advantages are reflected in the genetic structure of populations surrounding this area. Here, we used microsatellite genotype data to evaluate the structure and composition of baboon populations in southern Kenya. Our results indicate that, unlike for mitochondrial DNA, microsatellite-based measures of genetic structure concord with phenotypically based taxonomic distinctions and that the currently active hybrid zone is relatively narrow. Isolation with migration analysis revealed asymmetric gene flow in this region from anubis populations into yellow populations, in support of the anubis-biased phenotypic advantages observed in Amboseli. Populations that are primarily yellow but that receive anubis gene flow exhibit higher levels of genetic diversity than yellow populations far from the introgression front. Our results support previous work that indicates a long history of hybridization and introgression among East African baboons. Specifically, it suggests that anubis baboons are in the process of gradual range expansion into the range of yellow baboons, a pattern potentially explained by behavioural and life history advantages that correlate with anubis ancestry.
Sweet potato (Ipomoea batatas (L.) Lam., Convolvulaceae) counts among the most widely cultivated staple crops worldwide, yet the origins of its domestication remain unclear. This hexaploid species could have had either an autopolyploid origin, from the diploid I. trifida, or an allopolyploid origin, involving genomes of I. trifida and I. triloba. We generated molecular genetic data for a broad sample of cultivated sweet potatoes and its diploid and polyploid wild relatives, for noncoding chloroplast and nuclear ITS sequences, and nuclear SSRs. Our data did not support an allopolyploid origin for I. batatas, nor any contribution of I. triloba in the genome of domesticated sweet potato. I. trifida and I. batatas are closely related although they do not share haplotypes. Our data support an autopolyploid origin of sweet potato from the ancestor it shares with I. trifida, which might be similar to currently observed tetraploid wild Ipomoea accessions. Two I. batatas chloroplast lineages were identified. They show more divergence with each other than either does with I. trifida. We thus propose that cultivated I. batatas have multiple origins, and evolved from at least two distinct autopolyploidization events in polymorphic wild populations of a single progenitor species. Secondary contact between sweet potatoes domesticated in Central America and in South America, from differentiated wild I. batatas populations, would have led to the introgression of chloroplast haplotypes of each lineage into nuclear backgrounds of the other, and to a reduced divergence between nuclear gene pools as compared with chloroplast haplotypes.
The life cycles and dispersal of edible fungi are still poorly known, thus limiting our understanding of their evolution and domestication. The prized Tuber melanosporum produces fruitbodies (fleshy organs where meiospores mature) gathered in natural, spontaneously inoculated forests or harvested in plantations of nursery-inoculated trees. Yet, how fruitbodies are formed remains unclear, thus limiting yields, and how current domestication attempts affect population genetic structure is overlooked. Fruitbodies result from mating between two haploid individuals: the maternal parent forms the flesh and the meiospores, while the paternal parent only contributes to the meiospores. We analyzed the genetic diversity of T. melanosporum comparatively in spontaneous forests vs. plantations, using SSR polymorphism of 950 samples from South-East France. All populations displayed strong genetic isolation by distance at the metric scale, possibly due to animal dispersal, meiospore persistence in soil, and/or exclusion of unrelated individuals by vegetative incompatibility. High inbreeding was consistently found, suggesting that parents often develop from meiospores produced by the same fruitbody. Unlike maternal genotypes, paternal mycelia contributed to few fruitbodies each, did not persist over years, and were undetectable on tree mycorrhizae. Thus, we postulate that germlings from the soil spore bank act as paternal partners. Paternal genetic diversity and outbreeding were higher in plantations than in spontaneous truffle-grounds, perhaps because truffle growers disperse fruitbodies to maintain inoculation in plantations. However, planted and spontaneous populations were not genetically isolated, so that T. melanosporum illustrates an early step of domestication where genetic structure remains little affected.
Mitochondrial markers are still often used alone to identify evolutionary units, despite widespread evidence for processes such as incomplete lineage sorting or introgressive hybridization that may blur past population history. The combination of mitochondrial DNA data with other sources of information (morphology, nuclear genes) is a powerful tool to reveal when and why mitochondrial markers are potentially misleading. In this study, we evaluate the performance of mtDNA markers to unravel the evolutionary history of Spanish lizards from the Podarcis hispanicus species complex. We first uncover several cases of discordance between morphological and mitochondrial data in delimitation of taxa. To assess the origin of these discordances, we analysed the same populations using several independent nuclear loci. Both morphological and nuclear markers identified the same three evolutionary units in the region, while mitochondrial data revealed four deeply divergent lineages. We suggest here that the most likely scenario to explain this discordance is ancient mitochondrial introgression originating from a fourth evolutionary unit presently absent from the study area. Notably, this resulted in a complete replacement of the original lineage in a large part of the distribution of one of the taxa investigated. We discuss the potential evolutionary scenarios leading to this complete mitochondrial replacement and suggest why the previous studies have failed to recover the correct history of this species complex.
Mandrills (Mandrillus sphinx) are enigmatic Old World primates whose social organization and ecology remain poorly known. Previous studies indicated, for example, that groups are composed of only adult females and their young or that several units composed of one adult male and several females make up larger permanent social units. Here, we present the first data on group composition and male ranging patterns from the only habituated wild mandrill group and examine how home range size and daily path length varied with environmental and demographic factors over a 15-month period. Our study site is located in southern Gabon where we followed the group on a daily basis, collecting data on presence, ranging, behavior, and parasite load of its individual members. Throughout the study, the group was made up of about 120 individuals, including several non-natal and natal adult and sub-adult males. One-male units were never observed. The mandrills traveled an estimated 0.44-6.50 km/day in a home range area of 866.7 ha. Exploratory analyses revealed that precipitation, the number of adult males present, and the richness of protozoan parasites were all positively correlated with daily path length. These results clarify the social system of mandrills and provide first insights into the factors that shape their ranging patterns.
How do invasive pests affect interactions between members of pre-existing agrosystems? The invasive pest Drosophila suzukii is suspected to be involved in the aetiology of sour rot, a grapevine disease that otherwise develops following Drosophila melanogaster infestation of wounded berries. We combined field observations with laboratory assays to disentangle the relative roles of both Drosophila in disease development. We observed the emergence of numerous D. suzukii, but no D. melanogaster flies, from bunches that started showing mild sour rot symptoms days after field collection. However, bunches that already showed severe rot symptoms in the field mostly contained D. melanogaster. In the laboratory, oviposition by D. suzukii triggered sour rot development. An independent assay showed the disease increased grape attractiveness to ovipositing D. melanogaster females. Our results suggest that in invaded vineyards, D. suzukii facilitates D. melanogaster infestation and, consequently, favours sour rot outbreaks. Rather than competing with close species, the invader subsequently permits their reproduction in otherwise non-accessible resources and may cause more frequent, or more extensive, disease outbreaks.
Hybridization has played a central role in the evolutionary history of domesticated plants. Notably, several breeding programs relying on gene introgression from the wild compartment have been performed in fruit tree species within the genus Prunus but few studies investigated spontaneous gene flow among wild and domesticated Prunus species. Consequently, a comprehensive understanding of genetic relationships and levels of gene flow between domesticated and wild Prunus species is needed. Combining nuclear and chloroplastic microsatellites, we investigated the gene flow and hybridization among two key almond tree species, the cultivated Prunus dulcis and one of the most widespread wild relative Prunus orientalis in the Fertile Crescent. We detected high genetic diversity levels in both species along with substantial and symmetric gene flow between the domesticated P. dulcis and the wild P. orientalis. These results were discussed in light of the cultivated species diversity, by outlining the frequent spontaneous genetic contributions of wild species to the domesticated compartment. In addition, crop-to-wild gene flow suggests that ad hoc transgene containment strategies would be required if genetically modified cultivars were introduced in the northwestern Mediterranean.
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