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Lemmon, E. M.

Publications and source records attributed to Lemmon, E. M..

10 recordsLinked to original sources

Phylogenomic assessment of microhylid frogs reveals widespread taxonomic confusion in the Asterophryinae and establishes the timing of diversification in Australia

Microhylid frogs are a hyper-diverse family thought to have radiated explosively around the Cretaceous-Paleogene boundary. Roughly half of microhylid species richness is concentrated into a single subfamily, the Asterophryinae, which is centered in New Guinea and surrounds, and has been a rich source for species discovery over the past 50 years. However, resolving Asterophryinae phylogenetics has remained a challenge, with frequent taxonomic reshuffling. To address this instability, we generated a sequence-capture molecular dataset to investigate the phylogenetics of the group. This included 71 species of Asterophryinae, across 13 of 17 recognized genera representing extensive sampling of the New Guinea radiation and full sampling of Australian microhylid species. Our dated species tree supports an explosive diversification of microhylids in New Guinea near the start of the Miocene, approximately 20 million years ago. Asterophryinae expansion into northern Australia occurred much later ([~]10 ma) and is marked by well supported clades of Austrochaperina and Cophixalus that show temporally consistent splits from their New Guinea sister taxa. Our phylogeny allows us to identify several instances of polyphyly, which are at odds with our current understanding of intergeneric relationships within the Asterophryinae. We suggest that this confusion is a result of rapid radiation and morphological variability across some poorly defined genera. This work establishes a reliable phylogenetic framework that can form a foundation for a more stable taxonomy of the Asterophryinae. HighlightsO_LIA phylogenomic assessment of the globally distributed frog family Microhylidae C_LIO_LIThe subfamily Asterophryinae radiated explosively in New Guinea C_LIO_LIAustralian species represent two distinct clades C_LIO_LIAssignments of species to genera by morphological means are often unreliable C_LI

evolutionary biology↗

Loss of a morph is associated with asymmetric character release in a radiation of woodland salamanders

Color polymorphism, the occurrence of multiple discrete color morphs with co-adapted sets of traits within the same population, may provide the raw materials for rapid species formation. It has been hypothesized that fixation of a single morph can result in character release, whereby the monomorphic form evolves without the constraint of accommodating multiple adaptive peaks. However, the rates of evolution between populations fixed for different morphs likely depend on the specific adaptive zones occupied by each morph. We studied the evolution of dorsal color polymorphism (striped and unstriped morphs) in woodland salamanders (Plethodon), a North American radiation in which the polymorphism can be found in even the most distantly related species ([~]44 Ma divergence). We estimated a phylogenomic tree of Plethodon, representing all extant taxa with multiple samples for most species. Morphometric data suggest that between-species variation exists predominantly along an axis of relative body elongation, likely corresponding to a terrestrial-fossorial continuum. Polymorphic species occupy an intermediate phenotypic space between the evolutionary optima of striped and unstriped species, although polymorphic species did not have elevated speciation rates. Faster rates of body shape evolution were observed in unstriped species, suggesting that body elongation, which is co-adapted with the unstriped morph, is constrained by the polymorphism. Striped species had slower rates of evolution than polymorphic species, despite lacking the genetic constraints often associated with polymorphism. Our results demonstrate that rates of phenotypic evolution and speciation following character release can be asymmetric and idiosyncratic depending on the alternative adaptations of each morph.

evolutionary biology↗

Not one, but multiple radiations underlie the biodiversity of Madagascar's endangered lemurs

Lemurs are often cited as an example of adaptive radiation. Since colonizing Madagascar, more than 100 extant lemur species have evolved to fill a variety of ecological niches on the island. However, recent work suggests that lemurs do not exhibit one of the hallmarks of other adaptive radiations: explosive speciation rates that decline over time. Thus, characterizing the tempo and mode of evolution in lemurs can help us understand alternative ways that hyperdiverse clades arise over time, which might differ from traditional models. We explore the evolution of lemurs using a phylogenomic dataset with broad taxonomic sampling that includes the lemurs sister group, the lorisiforms of Asia and continental Africa. Our analyses reveal multiple bursts of diversification (without subsequent declines) that explain much of todays lemur diversity. We also find higher rates of speciation in Madagascars lemurs compared to lorisiforms, and we demonstrate that the lemur clades with exceptionally high diversification rates have higher rates of genomic introgression. This suggests that hybridization in these primates is not an evolutionary dead-end, but a driving force for diversification. Considering the conservation crisis affecting strepsirrhine primates, with approximately 95% of species being threatened with extinction, this phylogenomic study offers a new perspective for explaining Madagascars exceptional primate diversity and reveals patterns of speciation, extinction, and gene flow that will help inform future conservation decisions.

evolutionary biology↗

Biogeography and the evolution of acoustic communication in the polyploid North American gray treefrog complex

After polyploid species are formed, interactions between diploid and polyploid lineages may generate additional diversity in novel cytotypes and phenotypes. In anurans, mate choice by acoustic communication is the primary method by which individuals identify their own species and assess suitable mates. As such, the evolution of acoustic signals is an important mechanism for contributing to reproductive isolation and diversification in this group. Here, we estimate the biogeographic history of the North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid Hyla versicolor, focusing specifically on the geographic origin of whole genome duplication and the expansion of lineages out of glacial refugia. We then test for lineage-specific differences in mating signals by applying comparative methods to a large acoustic data set collected over 52 years that includes >1500 individual frogs. Along with describing the overall biogeographic history and call diversity, we found evidence that the geographic origin of H. versicolor and the formation of the midwestern polyploid lineage are both associated with glacial limits, and that the southwestern polyploid lineage is associated with a shift in acoustic phenotype relative to the diploid lineage with which they share a mitochondrial lineage. In H. chrysoscelis, we see that acoustic signals are largely split by Eastern and Western lineages, but that northward expansion along either side of the Appalachian Mountains is associated with further acoustic diversification. Overall, results of this study provide substantial clarity on the evolution of gray treefrogs as it relates to their biogeography and acoustic communication.

evolutionary biology↗

The complex history of genome duplication andhybridization in North American gray treefrogs

Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. While systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencing technology have demonstrated that conclusions from data-limited studies may be spurious and misleading. The North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid Hyla versicolor, has long been used as a model system in a variety of biological fields, yet all taxonomic studies to date were conducted with only a few loci from nuclear and mitochondrial genomes. Here, we utilized anchored hybrid enrichment and high-throughput sequencing to capture hundreds of loci along with whole mitochondrial genomes to investigate the evolutionary history of this complex. We used several phylogenetic and population genetic methods, including coalescent simulations and testing of polyploid speciation models with Approximate Bayesian Computation (ABC), to determine that H. versicolor was most likely formed via autopolyploidization from a now extinct lineage of H. chrysoscelis. We also uncovered evidence of significant hybridization between diploids and tetraploids where they co-occur, and show that historical hybridization between these groups led to the re-formation of distinct polyploid lineages following the initial whole genome duplication event. Our study indicates that a wide variety of methods and explicit model testing of polyploid histories can greatly facilitate efforts to uncover the evolutionary history of polyploid complexes.

genomics↗

Gene flow in phylogenomics: Sequence capture resolves species limits and biogeography of Afromontane forest endemic frogs from the Cameroon Highlands

Puddle frogs of the Phrynobatrachus steindachneri species complex are a useful group for investigating speciation and phylogeography in Afromontane forests of the Cameroon Highlands (Cameroon Volcanic Line) in western Central Africa. The species complex is represented by six morphologically relatively cryptic mitochondrial DNA lineages, with only two of them distinguished at the species level - southern P. jimzimkusi and Lake Oku endemic P. njiomock, leaving the remaining four lineages with a pooled identification as P. steindachneri. In this study, the six mtDNA lineages are subjected to genomic sequence capture analyses to delimit species (together with morphology) and to study biogeography. Nuclear DNA data (387 loci; 571,936 aligned base pairs) distinguished all six mtDNA lineages, but the splitting pattern and depths of divergences supported only four main clades--besides P. jimzimkusi and P. njiomock, only two from the four P. steindachneri mtDNA lineages. One is here described as a new species, P. sp. nov. Reticulate evolution (hybridization) was detected within the species complex with morphologically intermediate hybrid individuals placed between the parental species in phylogenomic analyses, forming a phylogenetic artefact - a ladder-like tree pattern. The presence of hybrids is undesirable in standard phylogenetic analyses, but is essential and beneficial in the network multispecies coalescent. This latter approach allowed us an insight into the reticulate evolutionary history of these endemic frogs. Introgressions likely occurred during the Middle and Late Pleistocene climatic oscillations, due to the cyclic connections (likely dominating during cold glacials) and separations (warm interglacials) of montane forests. The genomic phylogeographic pattern supports the earliest division between southern (Mt. Manengouba to Mt. Oku) and northern mountains at the onset of the Pleistocene. Further subdivisions occurred in the Early Pleistocene separating populations from the northernmost (Tchabal Mbabo, Gotel Mts.) and middle mountains (Mt. Mbam, Mt. Oku, Mambilla Plateau), as well as the microendemic lineage restricted to Lake Oku (Mt. Oku). Mount Oku harboring three species is of particular conservation importance. This unique model system is highly threatened as all the species within the complex have exhibited severe population declines in the past decade, placing them on the brink of extinction. We therefore urge for conservation actions in the Cameroon Highlands to preserve their diversity before it is too late.

evolutionary biology↗

The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order alone includes nine of the top ten most unstable nodes in angiosperms, and the recalcitrant relationships along the backbone of the order have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 15%, 52%, and 32% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

evolutionary biology↗

Whole genome duplication potentiates inter-specific hybridisation and niche shifts in Australian burrowing frogs Neobatrachus

Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less well-understood. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful animal polyploid model system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin and inheritance mode of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We resolve the phylogenetic relationships among Neobatrachus species and provide further support that the three polyploid species have independent autotetraploid origins. We document higher genetic diversity in tetraploids, resulting from widespread gene flow specifically between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and current isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate variation on frogs with differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which in turn corresponds to population genomic estimates of demographic histories. We propose that Neobatrachus diploids may be suffering the early genomic impacts of climate-induced habitat loss, while tetraploids appear to be avoiding this fate, possibly due to widespread gene flow into tetraploid lineages specifically. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on the evolution of adaptation in animals.

evolutionary biology↗

Resolving Rapid Radiations Within Families Using Anchored Phylogenomics

Despite the promise that molecular data would provide a seemingly unlimited source of independent characters, many plant phylogenetic studies are based on only two regions, the plastid genome and nuclear ribosomal DNA (nrDNA). Their popularity can be explained by high copy numbers and universal PCR primers that make their sequences easily amplified and converted into parallel datasets. Unfortunately, their utility is limited by linked loci and limited characters resulting in low confidence in the accuracy of phylogenetic estimates, especially when rapid radiations occur. In another contribution on anchored phylogenomics in angiosperms, we presented flowering plant-specific anchored enrichment probes for hundreds of conserved nuclear genes and demonstrated their use at the level of all angiosperms. In this contribution, we focus on a common problem in phylogenetic reconstructions below the family level: weak or unresolved backbone due to rapid radiations ([≤] 10 million years) followed by long divergence, using the Cariceae-Dulichieae-Scirpeae clade (CDS, Cyperaceae) as a test case. By comparing our nuclear matrix of 461 genes to a typical Sanger-sequence dataset consisting of a few plastid genes (matK, ndhF) and an nrDNA marker (ETS), we demonstrate that our nuclear data is fully compatible with the Sanger dataset and resolves short backbone internodes with high support in both concatenated and coalescence-based analyses. In addition, we show that nuclear gene tree incongruence is inversely proportional to phylogenetic information content, indicating that incongruence is mostly due to gene tree estimation error. This suggests that large numbers of conserved nuclear loci could produce more accurate trees than sampling rapidly evolving regions prone to saturation and long-branch attraction. The robust phylogenetic estimates obtained here, and high congruence with previous morphological and molecular analyses, are strong evidence for a complete tribal revision of CDS. The anchored hybrid enrichment probes used in this study should be similarly effective in other flowering plant groups. [Carex, coalescent based species tree, flowering plants, low-copy nuclear genes, low-level phylogenetics, universal hybrid enrichment probes]

plant biology↗

Anchored Phylogenomics of Angiosperms I: Assessing the Robustness of Phylogenetic Estimates

An important goal of the angiosperm systematics community has been to develop a shared approach to molecular data collection, such that phylogenomic data sets from different focal clades can be combined for meta-studies across the entire group. Although significant progress has been made through efforts such as DNA barcoding, transcriptome sequencing, and whole-plastid sequencing, the community current lacks a cost efficient methodology for collecting nuclear phylogenomic data across all angiosperms. Here, we leverage genomic resources from 43 angiosperm species to develop enrichment probes useful for collecting ~500 loci from non-model taxa across the diversity of angiosperms. By taking an anchored phylogenomics approach, in which probes are designed to represent sequence diversity across the group, we are able to efficiently target loci with sufficient phylogenetic signal to resolve deep, intermediate, and shallow angiosperm relationships. After demonstrating the utility of this resource, we present a method that generates a heat map for each node on a phylogeny that reveals the sensitivity of support for the node across analysis conditions, as well as different locus, site, and taxon schemes. Focusing on the effect of locus and site sampling, we use this approach to statistically evaluate relative support for the alternative relationships among eudicots, monocots, and magnoliids. Although the results from supermatrix and coalescent analyses are largely consistent across the tree, we find support for this deep relationship to be more sensitive to the particular choice of sites and loci when a supermatrix approach as employed. Averaged across analysis approaches and data subsampling schemes, our data support a eudicot-monocot sister relationship, which is supported by a number of recent angiosperm studies.

evolutionary biology↗