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1. Gene Flow Increases Phylogenetic Structure and Inflates Cryptic Species Estimations: A Case Study on Widespread Philippine Puddle Frogs ( Occidozyga laevis )

   https://doi.org/10.1093/sysbio/syab034  

   Chan, Kin Onn ; Hutter, Carl R ; Wood, Perry L ; Su, Yong-Chao ; Brown, Rafe M ( May 2021 , Systematic Biology)

   Burbrink, Frank (Ed.)

   Abstract In cryptic amphibian complexes, there is a growing trend to equate high levels of genetic structure with hidden cryptic species diversity. Typically, phylogenetic structure and distance-based approaches are used to demonstrate the distinctness of clades and justify the recognition of new cryptic species. However, this approach does not account for gene flow, spatial, and environmental processes that can obfuscate phylogenetic inference and bias species delimitation. As a case study, we sequenced genome-wide exons and introns to evince the processes that underlie the diversification of Philippine Puddle Frogs—a group that is widespread, phenotypically conserved, and exhibits high levels of geographically based genetic structure. We showed that widely adopted tree- and distance-based approaches inferred up to 20 species, compared to genomic analyses that inferred an optimal number of five distinct genetic groups. Using a suite of clustering, admixture, and phylogenetic network analyses, we demonstrate extensive admixture among the five groups and elucidate two specific ways in which gene flow can cause overestimations of species diversity: 1) admixed populations can be inferred as distinct lineages characterized by long branches in phylograms; and 2) admixed lineages can appear to be genetically divergent, even from their parental populations when simple measures of genetic distance are used. We demonstrate that the relationship between mitochondrial and genome-wide nuclear $p$-distances is decoupled in admixed clades, leading to erroneous estimates of genetic distances and, consequently, species diversity. Additionally, genetic distance was also biased by spatial and environmental processes. Overall, we showed that high levels of genetic diversity in Philippine Puddle Frogs predominantly comprise metapopulation lineages that arose through complex patterns of admixture, isolation-by-distance, and isolation-by-environment as opposed to species divergence. Our findings suggest that speciation may not be the major process underlying the high levels of hidden diversity observed in many taxonomic groups and that widely adopted tree- and distance-based methods overestimate species diversity in the presence of gene flow. [Cryptic species; gene flow; introgression; isolation-by-distance; isolation-by-environment; phylogenetic network; species delimitation.] 

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2. Ongoing hybridization obscures phylogenetic relationships in the Drosophila subquinaria species complex

   https://doi.org/10.1111/jeb.13512  

   Ginsberg, Paul S. ; Humphreys, Devon P. ; Dyer, Kelly A. ( August 2019 , Journal of Evolutionary Biology)

   Inferring evolutionary relationships among recently diverged lineages is necessary to understand how isolating barriers produce independent lineages. Here, we investigate the phylogenetic relationships between three incompletely isolated and closely related mushroom‐feedingDrosophilaspecies. These species form theDrosophila subquinariaspecies complex and consist of one Eurasian species (D. transversa) and two widespread North American species (D. subquinariaandD. recens) that are sympatric in central Canada. Although patterns of pre‐ and post‐mating isolation among these species are well characterized, previous work on their phylogenetic relationships is limited and conflicting. In this study, we generated a multi‐locus data set of 29 loci from across the genome sequenced in a population sample from each species, and then, we inferred species relationships and patterns of introgression. We find strong statistical support thatD. subquinariais paraphyletic, showing that samples from the geographic region sympatric withD. recensare most closely related toD. recens, whereas samples from the geographic region allopatric withD. recensare most closely related toD. transversa. We present several lines of evidence that both incomplete lineage sorting and gene flow are causing phylogenetic discordance. We suggest that ongoing gene flow primarily fromD. recensintoD. subquinariain the sympatric part of their ranges causes phylogenetic uncertainty in the evolutionary history of these species. Our results highlight how population genetic data can be used to disentangle the sources of phylogenetic discordance among closely related species.

    

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3. Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States

   https://doi.org/10.1093/gbe/evab260  

   Finger, Nicholas ; Farleigh, Keaka ; Bracken, Jason T ; Leaché, Adam D ; François, Olivier ; Yang, Ziheng ; Flouri, Tomas ; Charran, Tristan ; Jezkova, Tereza ; Williams, Dean A ; et al ( January 2022 , Genome Biology and Evolution)

   Baldauf, Sandra (Ed.)

   Abstract The southwestern and central United States serve as an ideal region to test alternative hypotheses regarding biotic diversification. Genomic data can now be combined with sophisticated computational models to quantify the impacts of paleoclimate change, geographic features, and habitat heterogeneity on spatial patterns of genetic diversity. In this study, we combine thousands of genotyping-by-sequencing (GBS) loci with mtDNA sequences (ND1) from the Texas horned lizard (Phrynosoma cornutum) to quantify relative support for different catalysts of diversification. Phylogenetic and clustering analyses of the GBS data indicate support for at least three primary populations. The spatial distribution of populations appears concordant with habitat type, with desert populations in AZ and NM showing the largest genetic divergence from the remaining populations. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype–environment association with bioclimatic variables supports divergence along precipitation gradients more than along temperature gradients. Demographic analyses support a complex history, with introgression and gene flow playing an important role during diversification. Bayesian multispecies coalescent analyses with introgression (MSci) analyses also suggest that gene flow occurred between populations. Paleo-species distribution models support two southern refugia that geographically correspond to contemporary lineages. We find that divergence times are underestimated and population sizes are overestimated when introgression occurred and is ignored in coalescent analyses, and furthermore, inference of ancient introgression events and demographic history is sensitive to inclusion of a single recently admixed sample. Our analyses cannot refute the riverine barrier or glacial refugia hypotheses. Results also suggest that populations are continuing to diverge along habitat gradients. Finally, the strong evidence of admixture, gene flow, and mtDNA introgression among populations suggests that P. cornutum should be considered a single widespread species under the General Lineage Species Concept. 

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4. Assessing models of speciation under different biogeographic scenarios; an empirical study using multi‐locus and RNA ‐seq analyses

   https://doi.org/10.1002/ece3.1865  

   Edwards, Taylor ; Tollis, Marc ; Hsieh, PingHsun ; Gutenkunst, Ryan N. ; Liu, Zhen ; Kusumi, Kenro ; Culver, Melanie ; Murphy, Robert W. ( January 2016 , Ecology and Evolution)

   Evolutionary biology often seeks to decipher the drivers of speciation, and much debate persists over the relative importance of isolation and gene flow in the formation of new species. Genetic studies of closely related species can assess if gene flow was present during speciation, because signatures of past introgression often persist in the genome. We test hypotheses on which mechanisms of speciation drove diversity among three distinct lineages of desert tortoise in the genusGopherus. These lineages offer a powerful system to study speciation, because different biogeographic patterns (physical vs. ecological segregation) are observed at opposing ends of their distributions. We use 82 samples collected from 38 sites, representing the entire species' distribution and generate sequence data for mtDNAand four nuclear loci. A multilocus phylogenetic analysis in *BEAST estimates the species tree.RNA‐seq data yield 20,126 synonymous variants from 7665 contigs from two individuals of each of the three lineages. Analyses of these data using the demographic inference package ∂a∂i serve to test the null hypothesis of no gene flow during divergence. The best‐fit demographic model for the three taxa is concordant with the *BEAST species tree, and the ∂a∂i analysis does not indicate gene flow among any of the three lineages during their divergence. These analyses suggest that divergence among the lineages occurred in the absence of gene flow and in this scenario the genetic signature of ecological isolation (parapatric model) cannot be differentiated from geographic isolation (allopatric model).

    

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5. Reproductive isolation and introgression between sympatric Mimulus species

   https://doi.org/10.1111/mec.13630  

   Kenney, Amanda M. ; Sweigart, Andrea L. ( May 2016 , Molecular Ecology)

   Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflowerMimulus guttatusand selfingM. nasutus. Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F₁‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus, demonstrating ongoing hybridization and asymmetric introgression fromM. nasutusintoM. guttatus. Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL, whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutusancestry inM. guttatusgenetic backgrounds. Together, our results suggest thatMimulusspeciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.

    

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