The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes.

Nitrogen-fixing symbiosis is globally important in ecosystem functioning and agriculture, yet the evolutionary history of nodulation remains the focus of considerable debate. Recent evidence suggesting a single origin of nodulation followed by massive parallel evolutionary losses raises questions about why a few lineages in the N2 -fixing clade retained nodulation and diversified as stable nodulators, while most did not. Within legumes, nodulation is restricted to the two most diverse subfamilies, Papilionoideae and Caesalpinioideae, which show stable retention of nodulation across their core clades. We characterize two nodule anatomy types across 128 species in 56 of the 152 genera of the legume subfamily Caesalpinioideae: fixation thread nodules (FTs), where nitrogen-fixing bacteroids are retained within the apoplast in modified infection threads, and symbiosomes, where rhizobia are symplastically internalized in the host cell cytoplasm within membrane-bound symbiosomes (SYMs). Using a robust phylogenomic tree based on 997 genes from 147 Caesalpinioideae genera, we show that losses of nodulation are more prevalent in lineages with FTs than those with SYMs. We propose that evolution of the symbiosome allows for a more intimate and enduring symbiosis through tighter compartmentalization of their rhizobial microsymbionts, resulting in greater evolutionary stability of nodulation across this species-rich pantropical legume clade.

Boliviadendron, a new segregate genus of mimosoid legume (Leguminosae, Caesalpinioideae, mimosoid clade) narrowly endemic to the interior Andean valleys of Bolivia.

Phylogenetic analyses of DNA sequence data sampling all species of Leucochloron alongside representatives of genera of the Inga and Albizia clades of the larger ingoid clade of mimosoid legumes (sensu Koenen et al. 2020) confirm the non-monophyly of the genus Leucochloron. We show that Leucochloronbolivianum is placed in the Albizia clade, while the remaining four species of Leucochloron are placed in the Inga clade, in line with previous results. To rectify this non-monophyly, L.bolivianum is segregated as the new genus, Boliviadendron, with a single species, Boliviadendronbolivianum, narrowly endemic to the interior Andean valleys of Bolivia. We illustrate this new segregate genus, present a map of its distribution and discuss the striking lack of morphological distinctions between Boliviadendron and Leucochloron, as well as the phylogenetic and morphological affinities of Boliviadendron to the genera Enterolobium and Albizia.

Mezcala - a new segregate genus of mimosoid legume (Leguminosae, Caesalpinioideae, mimosoid clade) narrowly endemic to the Balsas Depression in Mexico.

Recent results have demonstrated that the genus Desmanthus is non-monophyletic because the genus Kanaloa is nested within it, with a single species, Desmanthusbalsensis placed as sister to the clade comprising Kanaloa plus the remaining species of Desmanthus. Here we transfer D.balsensis to a new segregate genus Mezcala, discuss the morphological features supporting this new genus, present a key to distinguish Mezcala from closely related genera in the Leucaena subclade, and provide a distribution map of M.balsensis.

Pleistocene glacial cycles drive isolation, gene flow and speciation in the high-elevation Andes.

Mountain ranges are amongst the most species-rich habitats, with many large and rapid evolutionary radiations. The tempo and mode of diversification in these systems are key unanswered questions in evolutionary biology. Here we study the Andean Lupinus radiation to understand the processes driving very rapid diversification in montane systems. We use genomic and transcriptomic data of multiple species and populations, and apply phylogenomic and demographic analyses to test whether diversification proceeded without interspecific gene flow - as expected if Andean orogeny and geographic isolation were the main drivers of diversification - or if diversification was accompanied by gene flow, in which case other processes were probably involved. We uncover several episodes of gene flow between species, including very recent events likely to have been prompted by changes in habitat connectivity during Pleistocene glacial cycles. Furthermore, we find that gene flow between species was heterogeneously distributed across the genome. We argue that exceptionally fast diversification of Andean Lupinus was partly a result of Late Pleistocene glacial cycles, with associated cycles of expansion and contraction driving geographic isolation or secondary contact of species. Furthermore, heterogeneous gene flow across the genome suggests a role for selection and ecological speciation in rapid diversification in this system.

Lost crops of the Incas: Origins of domestication of the Andean pulse crop tarwi, Lupinus mutabilis.

PREMISE OF THE STUDY: The Andean highlands are a hotspot of domestication, yet our understanding of the origins of early Andean agriculture remains fragmentary. Key questions of where, when, how many times, and from what progenitors many Andean crops were domesticated remain unanswered. The Andean lupine crop tarwi (Lupinus mutabilis) is a regionally important pulse crop with exceptionally high seed protein and oil content and is the focus of modern breeding efforts, but its origins remain obscure. METHODS: A large genome-wide DNA polymorphism data set was generated using nextRADseq to infer relationships among more than 200 accessions of Andean Lupinus species, including 24 accessions of L. mutabilis and close relatives. Phylogenetic and demographic analyses were used to identify the likely progenitor of tarwi and elucidate the area and timing of domestication in combination with archaeological evidence. KEY RESULTS: We infer that tarwi was domesticated once in northern Peru, most likely in the Cajamarca region within, or adjacent to the extant distribution of L. piurensis, which is the most likely wild progenitor. Demographic analyses suggest that tarwi split from L. piurensis around 2600 BP and suffered a classical domestication bottleneck. The earliest unequivocal archaeological evidence of domesticated tarwi seeds is from the Mantaro Valley, central Peru ca. 1800 BP. CONCLUSIONS: A single origin of tarwi from L. piurensis in northern Peru provides a robust working hypothesis for the domestication of this regionally important crop and is one of the first clear-cut examples of a crop originating in the highlands of northern Peru.

Contrasting plant diversification histories within the Andean biodiversity hotspot.

The Andes are the most species-rich global biodiversity hotspot. Most research and conservation attention in the Andes has focused on biomes such as rain forest, cloud forest, and páramo, where much plant species diversity is the hypothesized result of rapid speciation associated with the recent Andean orogeny. In contrast to these mesic biomes, we present evidence for a different, older diversification history in seasonally dry tropical forests (SDTF) occupying rain-shadowed inter-Andean valleys. High DNA sequence divergence in Cyathostegia mathewsii, a shrub endemic to inter-Andean SDTF, indicates isolation for at least 5 million years of populations separated by only ca. 600 km of high cordillera in Peru. In conjunction with fossil evidence indicating the presence of SDTF in the Andes in the late Miocene, our data suggest that the disjunct small valley pockets of inter-Andean SDTF have persisted over millions of years. These forests are rich in endemic species but massively impacted, and merit better representation in future plans for science and conservation in Andean countries.

Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.

The relative importance of local ecological and larger-scale historical processes in causing differences in species richness across the globe remains keenly debated. To gain insight into these questions, we investigated the assembly of plant diversity in the Cerrado in South America, the world's most species-rich tropical savanna. Time-calibrated phylogenies suggest that Cerrado lineages started to diversify less than 10 Mya, with most lineages diversifying at 4 Mya or less, coinciding with the rise to dominance of flammable C4 grasses and expansion of the savanna biome worldwide. These plant phylogenies show that Cerrado lineages are strongly associated with adaptations to fire and have sister groups in largely fire-free nearby wet forest, seasonally dry forest, subtropical grassland, or wetland vegetation. These findings imply that the Cerrado formed in situ via recent and frequent adaptive shifts to resist fire, rather than via dispersal of lineages already adapted to fire. The location of the Cerrado surrounded by a diverse array of species-rich biomes, and the apparently modest adaptive barrier posed by fire, are likely to have contributed to its striking species richness. These findings add to growing evidence that the origins and historical assembly of species-rich biomes have been idiosyncratic, driven in large part by unique features of regional- and continental-scale geohistory and that different historical processes can lead to similar levels of modern species richness.

Serendipitous backyard hybridization and the origin of crops.

Backyard gardens, dump heaps, and kitchen middens are thought to have provided important venues for early crop domestication via generation of hybrids between otherwise isolated plant species. However, this process has rarely been demonstrated empirically. For the majority of polyploid crops, it remains uncertain to what extent hybridization and polyploidization preceded domestication or were precipitated by human activities. Using archaeological, ethnobotanical, geographical, and genetic data, we investigate the extent and significance of predomestication cultivation, backyard sympatry, and spontaneous hybridization for the Mimosoid legume tree Leucaena, which is used as a food crop throughout south-central Mexico. We show that predomestication cultivation was widespread, involved numerous independent transitions from the wild to cultivation, and resulted in extensive artificial sympatry of 2-6 species locally and 13 species in total. Using chloroplast and rapidly evolving nuclear-encoded DNA sequences, we demonstrate that hybridization in Leucaena has been extensive and complex, spawning a diverse set of novel hybrids as a result of juxtaposition of species in cultivation. The scale and complexity of hybridization in Leucaena is significantly greater than that documented for any other Mexican plant domesticates so far. However, there are striking parallels between Leucaena and the other major Mexican perennial domesticates Agave and Opuntia, which show very similar domestication via backyard hybridization pathways. Our results suggest that backyard hybridization has played a central role in Mesoamerican crop domestication and demonstrate that the simple step of bringing species together in cultivation can provide a potent trigger for domestication.

Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes.

Species radiations provide unique insights into evolutionary processes underlying species diversification and patterns of biodiversity. To compare plant diversification over a similar time period to the recent cichlid fish radiations, which are an order of magnitude faster than documented bird, arthropod, and plant radiations, we focus on the high-altitude flora of the Andes, which is the most species-rich of any tropical mountains. Because of the recent uplift of the northern Andes, the upland environments where much of this rich endemic flora is found have been available for colonization only since the late Pliocene or Pleistocene, 2-4 million years (Myr) ago. Using DNA sequence data we identify a monophyletic group within the genus Lupinus representing 81 species endemic to the Andes. The age of this clade is estimated to be 1.18-1.76 Myr, implying a diversification rate of 2.49-3.72 species per Myr. This exceeds previous estimates for plants, providing the most spectacular example of explosive plant species diversification documented to date. Furthermore, it suggests that the high cichlid diversification rates are not unique. Lack of key innovations associated with the Andean Lupinus clade suggests that diversification was driven by ecological opportunities afforded by the emergence of island-like habitats after Andean uplift. Data from other genera indicate that lupines are one of a set of similarly rapid Andean plant radiations, continental in scale and island-like in stimulus, suggesting that the high-elevation Andean flora provides a system that rivals other groups, including cichlids, for understanding rapid species diversification.

Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida.

Brazilian peppertree (Schinus terebinthifolius) is a woody perennial that has invaded much of Florida. This native of northeastern Argentina, Paraguay, and Brazil was brought as an ornamental to both the west and east coasts of Florida at the end of the 19th century. It was recorded as an invader of natural areas in the 1950s, and has since extended its range to cover over 280 000 ha. Our goals were to understand the history of this invasion, as one step toward understanding why this exotic was so successful, and ultimately to improve development of biological control agents. We sampled plants from the native and exotic ranges, particularly Florida, and genotyped these individuals at nuclear and chloroplast loci. Nuclear microsatellite and cpDNA loci reveal strong genetic population structure consistent with limited dispersal in the introduced and native ranges. Bayesian clustering of microsatellite data separates the east and west coast plants in Florida into distinct populations. The two chloroplast haplotypes found in Florida are also concordant with this separation: one predominates on the east coast, the other on the west coast. Analysis of samples collected in South America shows that haplotypes as distinct as the two in Florida are unlikely to have come from a single source population. We conclude that the genetic evidence supports two introductions of Brazilian peppertree into Florida and extensive hybridization between them. The west coast genotype likely came from coastal Brazil at about 27 degrees south, whereas the east coast genotype probably originated from another, as yet unidentified site. As a result of hybridization, the Florida population does not exhibit low genetic variation compared to populations in the native range, possibly increasing its ability to adapt to novel environments. Hybridization also has important consequences for the selection of biocontrol agents since it will not be possible to identify closely co-adapted natural enemies in the native range, necessitating more extensive host testing.