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1. Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

   https://doi.org/10.1371/journal.pgen.1009095  

   Nelson, Thomas C. ; Stathos, Angela M. ; Vanderpool, Daniel D. ; Finseth, Findley R. ; Yuan, Yao-wu ; Fishman, Lila ( February 2021 , PLOS Genetics)

   Buerkle, Alex (Ed.)

   Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species ) . Taxa within Erythranthe , particularly the parapatric and putatively sister species M . lewisii (bee-pollinated) and M . cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M . cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M . lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson’s D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M . lewisii and M . cardinalis . Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M . lewisii and Southern Californian M . parishii each carrying organelle genomes nested within respective sympatric M . cardinalis clades. A recent organellar transfer from M . cardinalis , an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M . parishii organelles in hybrids with M . lewisii . Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation. 

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2. Reticulate evolutionary history and extensive introgression in mosquito species revealed by phylogenetic network analysis

   https://doi.org/10.1111/mec.13544  

   Wen, Dingqiao ; Yu, Yun ; Hahn, Matthew W. ; Nakhleh, Luay ( March 2016 , Molecular Ecology)

   The role of hybridization and subsequent introgression has been demonstrated in an increasing number of species. Recently, Fontaineet al. (Science, 347, 2015, 1258524) conducted a phylogenomic analysis of six members of theAnopheles gambiaespecies complex. Their analysis revealed a reticulate evolutionary history and pointed to extensive introgression on all four autosomal arms. The study further highlighted the complex evolutionary signals that the co‐occurrence of incomplete lineage sorting (ILS) and introgression can give rise to in phylogenomic analyses. While tree‐based methodologies were used in the study, phylogenetic networks provide a more natural model to capture reticulate evolutionary histories. In this work, we reanalyse theAnophelesdata using a recently devised framework that combines the multispecies coalescent with phylogenetic networks. This framework allows us to captureILSand introgression simultaneously, and forms the basis for statistical methods for inferring reticulate evolutionary histories. The new analysis reveals a phylogenetic network with multiple hybridization events, some of which differ from those reported in the original study. To elucidate the extent and patterns of introgression across the genome, we devise a new method that quantifies the use of reticulation branches in the phylogenetic network by each genomic region. Applying the method to the mosquito data set reveals the evolutionary history of all the chromosomes. This study highlights the utility of ‘network thinking’ and the new insights it can uncover, in particular in phylogenomic analyses of large data sets with extensive gene tree incongruence.

    

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3. Distinguishing level-1 phylogenetic networks on the basis of data generated by Markov processes

   https://doi.org/10.1007/s00285-021-01653-8  

   Gross, Elizabeth ; van Iersel, Leo ; Janssen, Remie ; Jones, Mark ; Long, Colby ; Murakami, Yukihiro ( September 2021 , Journal of Mathematical Biology)

   Phylogenetic networks can represent evolutionary events that cannot be described by phylogenetic trees. These networks are able to incorporate reticulate evolutionary events such as hybridization, introgression, and lateral gene transfer. Recently, network-based Markov models of DNA sequence evolution have been introduced along with model-based methods for reconstructing phylogenetic networks. For these methods to be consistent, the network parameter needs to be identifiable from data generated under the model. Here, we show that the semi-directed network parameter of a triangle-free, level-1 network model with any fixed number of reticulation vertices is generically identifiable under the Jukes–Cantor, Kimura 2-parameter, or Kimura 3-parameter constraints.

    

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4. Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum

   https://doi.org/10.1093/aob/mcad069  

   Martínez-Gómez, Jesús ; Park, Seongjun ; Hartogs, Samantha R ; Soza, Valerie L ; Park, SeonJoo ; Di Stilio, Verónica S ( May 2023 , Annals of Botany)

   Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus additionally allows to test for specialization to pollination vectors in the absence of this feature. Methods We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits, followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion. Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness, and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments, and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny while longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions While detectable suites of integrated floral traits across Thalictrum correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying pollination mode evolution in Thalictrum, presumably via different paths from an ancestral mixed pollination state. 

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5. Genomic and transcriptomic resources for candidate gene discovery in the Ranunculids

   https://doi.org/10.1002/aps3.11407  

   Arias, Tatiana ; Riaño‐Pachón, Diego Mauricio ; Di Stilio, Verónica S. ( January 2021 , Applications in Plant Sciences)

   Multiple transitions from insect to wind pollination are associated with polyploidy and unisexual flowers inThalictrum(Ranunculaceae), yet the underlying genetics remains unknown. We generated a draft genome ofThalictrum thalictroides, a representative of a clade with ancestral floral traits (diploid, hermaphrodite, and insect pollinated) and a model for functional studies. Floral transcriptomes ofT. thalictroidesand of wind‐pollinated, andromonoeciousT. hernandeziiare presented as a resource to facilitate candidate gene discovery in flowers with different sexual and pollination systems.

   A draft genome ofT. thalictroidesand two floral transcriptomes ofT. thalictroidesandT. hernandeziiwere obtained from HiSeq 2000 Illumina sequencing and de novo assembly.

   TheT. thalictroidesde novo draft genome assembly consisted of 44,860 contigs (N50 = 12,761 bp, 243 Mbp total length) and contained 84.5% conserved embryophyte single‐copy genes. Floral transcriptomes contained representatives of most eukaryotic core genes, and most of their genes formed orthogroups.

   To validate the utility of these resources, potential candidate genes were identified for the different floral morphologies using stepwise data set comparisons. Single‐copy gene analysis and simple sequence repeat markers were also generated as a resource for population‐level and phylogenetic studies.

    

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