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Abstract Background and AimsNovel traits frequently evolve by co-opting existing genetic pathways through either the direct repurposing of existing genes or neofunctionalization of duplicated genes. Parasitism represents a major innovation in plants, in which a novel organ, the haustorium, evolved to penetrate hosts to extract water and nutrients. Previous studies hypothesized that haustoria-associated genes evolved primarily from root and pollen-associated pathways by neofunctionalization following genome duplications. MethodsTo examine the evolutionary origins of haustoria-associated genes, we generated a chromosome-scale reference genome of the hemiparasite Pedicularis groenlandica (Orobanchaceae) and sampled transcriptomes throughout haustorial development. We identified haustoria-associated genes; quantified the expression of these genes and their paralogues across non-haustorial tissues; and investigated overlap in haustoria-associated genes with publicly available haustorial transcriptomes in four additional parasitic plants. Key ResultsWe identified 5635 haustoria-associated genes in P. groenlandica. A greater proportion of these genes were associated with pollen tubes (67 %) than with roots (33 %), evidenced by being either differentially expressed in pollen tubes or nested within pollen tube-associated gene families, or both. Haustoria-associated genes with paralogues that arose after the evolution of parasitism in Orobanchaceae are more likely to be uniquely expressed in haustoria, consistent with neofunctionalization. ConclusionsOur results support evidence of both pleiotropy and neofunctionalization as mechanisms by which genetic pathways are co-opted for haustorial function. Haustoria-associated genes are highly lineage specific, highlighting a dynamic and ongoing process of independent haustorial co-option of gene functions among parasitic plant lineages. 

Summary The genusDelphiniumexemplifies the complexity of plant diversification in mountainous regions, where rapid speciation, hybridization, and morphological convergence frequently obscure species boundaries. The North American lineageDelphiniumsect.Diedropetalahas rapidly radiated across a range of ecological habitats, from alpine tundra to desert grasslands, forming an iconic component of western wild flower communities.Here, we present a genome‐scale phylogeny of 34 taxa using ddRAD‐seq data from 150 individuals sampled across their geographic ranges.Our results reveal strong phylogenetic structure corresponding to biogeographic regions, including several well‐supported clades that cut across existing taxonomic subsections, emphasizing the need for taxonomic revision. Hybridization and introgression are widespread, occurring both within and between these regional clades. Most species are connected through a syngameon‐like network of introgression, with few widespread species acting as central hubs. We describe six higher‐level clade names and use an agent‐based artificial intelligence analysis to identify morphological synapomorphies that align with our genomic findings.Our study demonstrates that geography and gene flow have played a dominant role in shaping the evolutionary history ofDelphiniumin North America, offering a framework for revising its taxonomy and informing future conservation efforts. 

Abstract PremiseCo‐occurring plant species that share generalist pollinators often exchange pollen. This heterospecific pollen transfer (HPT) impacts male and female reproductive success through pollen loss and reductions in seed set, respectively. The resulting fitness cost of HPT imposes selection on reproductive traits (e.g., floral color and shape), yet we currently lack strong predictors for the post‐pollination fate of heterospecific pollen, especially within community and phylogenetic contexts. MethodsWe investigated the fate of heterospecific pollen at three distinct stages of plant reproduction: (1) pollen germination on the stigma, (2) pollen tube growth in the style, and (3) fertilization of ovules. We experimentally crossed 11 naturally co‐flowering species in the subalpine meadows of the Colorado Rocky Mountains, across a spectrum of phylogenetic relatedness. Using generalized linear mixed models and generalized linear models, we evaluated the effect of parental species identity and phylogenetic relatedness on pollen tube growth at each reproductive stage. ResultsWe found that heterospecific pollen tubes can germinate and grow within pistils at each reproductive stage, even when parental species are >100 My divergent. There was no significant effect of phylogenetic distance on heterospecific pollen success, and no evidence for a mechanism that suspends heterospecific pollen germination or pollen tube growth within heterospecific stigmas or styles. ConclusionsOur results show that even in communities where HPT is common, pre‐zygotic post‐pollination mechanisms do not provide strong barriers to interspecific fertilization. HPT can result in the loss of ovules even between highly diverged plant species. 

Abstract Genomes are composed of a mosaic of segments inherited from different ancestors, each separated by past recombination events. Consequently, genealogical relationships among multiple genomes vary spatially across different genomic regions. Genealogical variation among unlinked (uncorrelated) genomic regions is well described for either a single population (coalescent) or multiple structured populations (multispecies coalescent). However, the expected similarity among genealogies at linked regions of a genome is less well characterized. Recently, an analytical solution was derived for the distribution of the waiting distance for a change in the genealogical tree spatially across a genome for a single population with constant effective population size. Here, we describe a generalization of this result in terms of the distribution of waiting distances between changes in genealogical trees and topologies for multiple structured populations with branch-specific effective population sizes (i.e., under the multispecies coalescent). We implemented our model in the Python package ipcoal and validated its accuracy against stochastic coalescent simulations. Using a novel likelihood framework, we show that tree and topology-change waiting distances in an ancestral recombination graph can be used to fit species tree model parameters, demonstrating an application of our model for developing new methods for phylogenetic inference. The multi-species sequentially Markov coalescent model presented here represents a major advance for linking local ancestry inference to hierarchical demographic models. 

Abstract A fundamental objective of evolutionary biology is to understand the origin of independently evolving species. Phylogenetic studies of species radiations rarely are able to document ongoing speciation; instead, modes of speciation, entailing geographic separation and/or ecological differentiation, are posited retrospectively. The Oreinotinus clade of Viburnum has radiated recently from north to south through the cloud forests of Mexico and Central America to the Central Andes. Our analyses support a hypothesis of incipient speciation in Oreinotinus at the southern edge of its geographic range, from central Peru to northern Argentina. Although several species and infraspecific taxa have been recognized in this area, multiple lines of evidence and analytical approaches (including analyses of phylogenetic relationships, genetic structure, leaf morphology, and climatic envelopes) favor the recognition of just a single species, V. seemenii. We show that what has previously been recognized as V. seemenii f. minor has recently occupied the drier Tucuman-Bolivian forest region from Samaipata in Bolivia to Salta in northern Argentina. Plants in these populations form a well-supported clade with a distinctive genetic signature and they have evolved smaller, narrower leaves. We interpret this as the beginning of a within-species divergence process that has elsewhere in the neotropics resulted repeatedly in Viburnum species with a particular set of leaf ecomorphs. Specifically, the southern populations are in the process of evolving the small, glabrous, and entire leaf ecomorph that has evolved in four other montane areas of endemism. As predicted based on our studies of leaf ecomorphs in Chiapas, Mexico, these southern populations experience generally drier conditions, with large diurnal temperature fluctuations. In a central portion of the range of V. seemenii, characterized by wetter climatic conditions, we also document what may be the initial differentiation of the leaf ecomorph with larger, pubescent, and toothy leaves. The emergence of these ecomorphs thus appears to be driven by adaptation to subtly different climatic conditions in separate geographic regions, as opposed to parapatric differentiation along elevational gradients as suggested by Viburnum species distributions in other parts of the neotropics. 

Premise: Detecting historical introgression among populations or species from genomic data is a common goal in evolutionary genetics. Most current methods fall into two major categories: network inference and admixture inference. Network inference (e.g., SNaQ) is computationally challenging and typically requires first reducing large genomic datasets into a less informative collection of inferred gene trees. In contrast, admixture inference (e.g., ABBA‐BABA tests) can accommodate enormous single‐nucleotide polymorphism (SNP) data sets but is restricted to ex- amining subsets of four to five samples at a time. Here, we demonstrate a new approach to evaluate SNP frequencies among quartet samples under a phylogenetic hypothesis (similar to ABBA‐BABA tests), while examining all quartet information simultaneously (similar to the network inference methods). Methods and Results: To do this, our method simcat trains a neural network machine learning model on coalescent simulations to discriminate between intro- gression scenarios based on learned SNP frequency patterns. We demonstrate the accuracy of simcat to classify introgression events from simulations, evaluate its sensitivity to variation in species tree parameters, and demonstrate its application to an empirical data set of oak trees (Quercus ser. Virentes). Conclusions: Our approach represents a first step towards leveraging machine learning to expand phylogenetic invariants–based methods beyond the scale of quartets to a larger phylogenetic context. 

Here we use population genomic data (ddRAD-Seq) and ecological niche modeling to test biogeographic hypotheses for the divergence of the island-endemic cactus species Cereus insularis Hemsl. (Cereeae; Cactaceae) from its sister species C. fernambucensis Lem. The Cereus insularis grows in the Fernando de Noronha Islands (FNI), a Neotropical archipelago located 350 km off the Brazilian Atlantic Forest (BAF) coast. Phylogeographic reconstructions support a northward expansion by the common ancestor of C. insularis and C. fernambucensis along the mainland BAF coast, with C. insularis diverging from the widespread mainland taxon C. fernambucensis after colonizing FNI in the late Pleistocene. The morphologically distinct C. insularis is monophyletic and nested within C. fernambucensis, as expected from a progenitor-derivative speciation model. We tested alternative biogeographic and demographic hypotheses for the colonization of the FNI using Approximate Bayesian Computation. We found the greatest support for a stepping-stone path that emerged during periods of decreased sea level (the “bridge” hypothesis), in congruence with historical ecological niche modeling that shows highly suitable habitats on stepping-stone islands during glacial periods. The outlier analyses reveal signatures of selection in C. insularis, suggesting a putative role of adaptation driving rapid anagenic differentiation of this species in FNI. 

Orobanchaceae is the largest family of parasitic plants, containing autotrophic and parasitic plants with all degrees of parasitism. This makes it by far the best family for studying the origin and evolution of plant parasitism. Here we provide three high-quality genomes of orobanchaceous plants, the autotrophic Lindenbergia luchunensis and the holoparasitic plants Phelipanche aegyptiaca and Orobanche cumana. Phylogenomic analysis of these three genomes together with those previously published and the transcrip- tomes of other orobanchaceous species created a robust phylogenetic framework for Orobanchaceae. We found that an ancient whole-genome duplication (WGD; about 73.48 million years ago), which occurred earlier than the origin of Orobanchaceae, might have contributed to the emergence of parasitism. However, no WGD events occurred in any lineage of orobanchaceous parasites except for Striga after divergence from their autotrophic common ancestor, suggesting that, in contrast with previous speculations, WGD is not associated with the emergence of holoparasitism. We detected evident convergent gene loss in all parasites within Orobanchaceae and between Orobanchaceae and dodder Cuscuta australis. The gene families in the orobanchaceous parasites showed a clear pattern of recent gains and expansions. The expanded gene families are enriched in functions related to the development of the haustorium, sug- gesting that recent gene family expansions may have facilitated the adaptation of orobanchaceous parasites to different hosts. This study illustrates a stepwise pattern in the evolution of parasitism in the orobanchaceous parasites and will facilitate future studies on parasitism and the control of parasitic plants in agriculture.