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

   KIN ONN CHAN, CARL R. ( January 2021 , Systematic biology)

   null (Ed.)

   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 specificways in which gene flowcan 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-bydistance, 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. 

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

   KIN ONN CHAN, CARL R. ( January 2021 , Systematic biology)

   null (Ed.)

   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 specificways in which gene flowcan 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-bydistance, 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. 

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4. Notes from the taxonomic disaster zone: Evolutionary drivers of intractable species boundaries in an Australian lizard clade (Scincidae: Ctenotus )

   https://doi.org/10.1111/mec.17074  

   Prates, Ivan ; Hutchinson, Mark N. ; Singhal, Sonal ; Moritz, Craig ; Rabosky, Daniel L. ( July 2023 , Molecular Ecology)

   Genomic‐scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a “worst‐case” scenario for species delimitation within vertebrates: theCtenotus inornatusspecies group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation‐by‐distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that “taxonomic disaster zones” like theC. inornatusspecies group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.

    

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5. Global species delimitation and phylogeography of the circumtropical ‘sexy shrimp’ Thor amboinensis reveals a cryptic species complex and secondary contact in the Indo‐West Pacific

   https://doi.org/10.1111/jbi.13231  

   Titus, Benjamin M. ; Daly, Marymegan ; Hamilton, Natalie ; Berumen, Michael L. ; Baeza, J. Antonio ( April 2018 , Journal of Biogeography)

   The “sexy shrimp”Thor amboinensisis currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis thatT. amboinensisis a single global species, reconstruct its global biogeographical history, and comment on population‐level patterns throughout the Tropical Western Atlantic.

   Coral reefs in all tropical oceans.

   Specimens ofThor amboinensiswere obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in theTWAwas based onCOIonly (n = 303 individuals, 10 sample localities).

   We found evidence for at least five cryptic lineages (9%–22%COIpairwise sequence divergence): four in the Indo‐West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co‐occurring lineage that is widespread throughout the Indo‐West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km.

   Thor amboinensisis a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo‐West Pacific. Nuclear‐ and mitochondrial‐ gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi‐locus analyses suggest thatT. amboinensisoriginated in the Tethys sea and dispersed into the Atlantic and Indo‐West Pacific through the Tethys seaway or, alternatively, originated in the Indo‐West Pacific and dispersed into the Atlantic around South Africa. Population‐level patterns in the Caribbean indicate extensive gene flow across the region.

    

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