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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)

   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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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 creates a mirage of cryptic species in a Southeast Asian spotted stream frog complex

   https://doi.org/10.1111/mec.15603  

   Chan, Kin O.; Hutter, Carl R.; Wood, Jr, Perry L.; Grismer, L. L.; Das, Indraneil; Brown, Rafe M. (September 2020, Molecular Ecology)

   Abstract Most new cryptic species are described using conventional tree‐ and distance‐based species delimitation methods (SDMs), which rely on phylogenetic arrangements and measures of genetic divergence. However, although numerous factors such as population structure and gene flow are known to confound phylogenetic inference and species delimitation, the influence of these processes is not frequently evaluated. Using large numbers of exons, introns, and ultraconserved elements obtained using the FrogCap sequence‐capture protocol, we compared conventional SDMs with more robust genomic analyses that assess population structure and gene flow to characterize species boundaries in a Southeast Asian frog complex (Pulchrana picturata). Our results showed that gene flow and introgression can produce phylogenetic patterns and levels of divergence that resemble distinct species (up to 10% divergence in mitochondrial DNA). Hybrid populations were inferred as independent (singleton) clades that were highly divergent from adjacent populations (7%–10%) and unusually similar (<3%) to allopatric populations. Such anomalous patterns are not uncommon in Southeast Asian amphibians, which brings into question whether the high levels of cryptic diversity observed in other amphibian groups reflect distinct cryptic species—or, instead, highly admixed and structured metapopulation lineages. Our results also provide an alternative explanation to the conundrum of divergent (sometimes nonsister) sympatric lineages—a pattern that has been celebrated as indicative of true cryptic speciation. Based on these findings, we recommend that species delimitation of continuously distributed “cryptic” groups should not rely solely on conventional SDMs, but should necessarily examine population structure and gene flow to avoid taxonomic inflation. 

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4. Unexpectedly high levels of lineage diversity in Sundaland Puddle Frogs (Dicroglossidae: Occidozyga Kuhl and Van Hasselt, 1822).

   Flury, J. (January 2021, Molecular phylogenetics and evolution)

   null (Ed.)

   One of the most urgent contemporary tasks for taxonomists and evolutionary biologists is to estimate the number of species on earth. Recording alpha diversity is crucial for protecting biodiversity, especially in areas of elevated species richness, which coincide geographically with increased anthropogenic environmental pressures - the world’s so-called biodiversity hotspots. Although the distribution of Puddle frogs of the genus Occidozyga in South and Southeast Asia includes five biodiversity hotspots, the available data on phylogeny, species diversity, and biogeography are surprisingly patchy. Samples analyzed in this study were collected throughout Southeast Asia, with a primary focus on Sundaland and the Philippines. A mitochondrial gene region comprising ~ 2000 bp of 12S and 16S rRNA with intervening tRNA Valine and three nuclear loci (BDNF, NTF3, POMC) were analyzed to obtain a robust, time-calibrated phylogenetic hypothesis. We found a surprisingly high level of genetic diversity within Occidozyga, based on uncorrected p-distance values corroborated by species delimitation analyses. This extensive genetic diversity revealed 29 evolutionary lineages, defined by the > 5% uncorrected p-distance criterion for the 16S rRNA gene, suggesting that species diversity in this clade of phenotypically homogeneous forms probably has been underestimated. The comparison with results of other anuran groups leads to the assumption that anuran species diversity could still be substantially underestimated in Southeast Asia in general. Many genetically divergent lineages of frogs are phenotypically similar, indicating a tendency towards extensive morphological conservatism. We present a biogeographic reconstruction of the colonization of Sundaland and nearby islands which, together with our temporal framework, suggests that lineage diversification centered on the landmasses of the northern Sunda Shelf. This remarkably genetically structured group of amphibians could represent an exceptional case for future studies of geographical structure and diversification in a widespread anuran clade spanning some of the most pronounced geographical barriers on the planet (e.g., Wallace’s Line). Studies considering gene flow, morphology, ecological and bioacoustic data are needed to answer these questions and to test whether observed diversity of Puddle frog lineages warrants taxonomic recognition. 

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5. Evidence supporting cryptic species within two sessile microinvertebrates, Limnias melicerta and L. ceratophylli (Rotifera, Gnesiotrocha)

   https://doi.org/10.1371/journal.pone.0205203  

   Azar Kordbacheh, Azar; Wallace, R.L.; Walsh, 2 (October 2018, PloS one)

   Munderloh, Ulrike Gertrud (Ed.)

   Microorganisms, including rotifers, are thought to be capable of long distance dispersal. Therefore, they should show little population genetic structure due to high gene flow. Nevertheless, substantial genetic structure has been reported among populations of many taxa. In rotifers, genetic studies have focused on planktonic taxa leaving sessile groups largely unexplored. Here, we used COI gene and ITS region sequences to study genetic structure and delimit cryptic species in two sessile species (Limnias melicerta [32 populations]; L. ceratophylli [21 populations]). Among populations, ITS region sequences were less variable as compared to those of the COI gene (ITS; L. melicerta: 0–3.1% and L. ceratophylli: 0–4.4%; COI; L. melicerta: 0–22.7% and L. ceratophylli: 0–21.7%). Moreover, L. melicerta and L. ceratophylli were not resolved in phylogenetic analyses based on ITS sequences. Thus, we used COI sequences for species delimitation. Bayesian Species Delimitation detected nine putative cryptic species within L. melicerta and four putative cryptic species for L. ceratophylli. The genetic distance in the COI gene was 0–15.4% within cryptic species of L. melicerta and 0.5–0.6% within cryptic species of L. ceratophylli. Among cryptic species, COI genetic distance ranged 8.1–21.9% for L. melicerta and 15.1–21.2% for L. ceratophylli. The correlation between geographic and genetic distance was weak or lacking; thus geographic isolation cannot be considered a strong driver of genetic variation. In addition, geometric morphometric analyses of trophi did not show significant variation among cryptic species. In this study we used a conservative approach for species delimitation, yet we were able to show that species diversity in these sessile rotifers is underestimated. 

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