MITOCHONDRIAL AND NUCLEAR PATTERNS OF CONFLICT AND CONCORDANCE AT THE GENE, GENOME, AND BEHAVIORAL SCALES IN \u3cem\u3eDESMOGNATHUS\u3c/em\u3e SALAMANDERS

Advancements in molecular sequencing have revealed unexpected cryptic genetic diversity and contrasting evolutionary histories within genes and between genomes of many organisms; often in disagreement with recognized taxonomy. Incongruent patterns between the mitochondrial and nuclear evolutionary history can have several plausible explanations, but widespread systematic conflict inevitably challenges our conceptions of species boundaries when there is discordance between coevolving and coinherited genomes. It is unknown to what degree mitonuclear conflict drives the process of divergence, or how ubiquitous these patterns are across the tree of life. To understand the evolutionary relevance of intergenomic discordance we must identify the conflicting patterns that exist in natural systems by generating robust estimates of the underlying species history, quantify support for alternative hypotheses of lineage formation, and describe patterns of genetic variation present in robust nuclear genomic datasets. Empirically testing correlations between mitonuclear genomic conflict and reduced gene flow at the organism level will contribute toward a better understanding of lineage boundaries and how intergenomic interactions shape the process of divergence. Mitochondrial introgression has been inferred in many salamander systems with limited perspective from nuclear sequence data. Within dusky salamanders (Desmognathus), these patterns have been observed between morphologically and geographically disparate populations. I sequenced regions throughout the nuclear genome to reconstruct species trees, performed population-level analyses testing concordance between the mitochondrial, nuclear datasets, and nuclear genes with mitochondrial functions with the expectation that coevolutionary interactions among genomes are more likely to manifest in these regions. I also estimated migration rates between populations that may have experienced historical mitochondrial introgression to evaluate phylogeographic patterns. Using these data we definitively reject species models in which genetic boundaries are based solely on mitochondrial data, favoring geographic models instead. Furthermore, analyses soundly reject current taxonomic models based on morphological characteristics, suggesting there is greater lineage diversity than is currently recognized. I also used empirical assays of pre-zygotic reproductive mating behavior within and among populations containing diverse mitochondrial lineages to test metrics of reproductive isolation, and to determine if introgression shapes the evolution of complex traits directly influencing rates of divergence. These results may explain incongruent patterns observed between the mitochondrial and nuclear data as a function of inheritance and population dynamics rather than directly functioning to suppress nuclear gene flow. This research builds upon recent studies suggesting that speciation is a highly complex and often non-bifurcating process in which introgression can have a profound and lasting signature on the nuclear evolutionary history. Mechanisms responsible for divergence with gene flow challenge evolutionary biologists to reevaluate our notions and definitions of species boundaries to accommodate seemingly conflicted genomic patterns within and between genomes

Phylogenomics Reveals Ancient Gene Tree Discordance in the Amphibian Tree of Life

The Author(s) 2020. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. Molecular phylogenies have yielded strong support for many parts of the amphibian Tree of Life, but poor support for the resolution of deeper nodes, including relationships among families and orders. To clarify these relationships, we provide a phylogenomic perspective on amphibian relationships by developing a taxon-specific Anchored Hybrid Enrichment protocol targeting hundreds of conserved exons which are effective across the class. After obtaining data from 220 loci for 286 species (representing 94% of the families and 44% of the genera), we estimate a phylogeny for extant amphibians and identify gene tree-species tree conflict across the deepest branches of the amphibian phylogeny. We perform locus-by-locus genealogical interrogation of alternative topological hypotheses for amphibian monophyly, focusing on interordinal relationships. We find that phylogenetic signal deep in the amphibian phylogeny varies greatly across loci in a manner that is consistent with incomplete lineage sorting in the ancestral lineage of extant amphibians. Our results overwhelmingly support amphibian monophyly and a sister relationship between frogs and salamanders, consistent with the Batrachia hypothesis. Species tree analyses converge on a small set of topological hypotheses for the relationships among extant amphibian families. These results clarify several contentious portions of the amphibian Tree of Life, which in conjunction with a set of vetted fossil calibrations, support a surprisingly younger timescale for crown and ordinal amphibian diversification than previously reported. More broadly, our study provides insight into the sources, magnitudes, and heterogeneity of support across loci in phylogenomic data sets.[AIC; Amphibia; Batrachia; Phylogeny; gene tree-species tree discordance; genomics; information theory.].This work was supported by grants from a graduate student research award from the Society of Systematic Biologists and the University of Kentucky G.F. Ribble Endowment (to P.M.H.), by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/BEX 2806/09-6 to P.L.V.P.), and by the National Science Foundation (DEB-0949532 and DEB-1355000 to D.W.W., DEB-1120516 to E.M.L., IIP-1313554 to A.R.L. and E.M.L, DEB-1355071 to J.M.B., DEB-1441719 to R.A.P., DEB-1311442 to P.L.V.P., DEB-1354506 to R.C.T., DEB-1021247 to E.P. and C.J.R., DEB-1021299 to K.M. Kjer, and DEB-1257610, DEB-0641023, DEB-0423286, and DEB-9984496 to C.J.R.), and the Australian Research Council (DP120104146 to J.S.K. and S.C.D.). S.R.R. thanks SENESCYT (Arca de Noé Initiative; SRR and O. Torres-Carvajal principal investigators) for funding for tissue collection. J.L. was supported by the Systematics Association and the Linnean Society Systematics Research Fund. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program (DGE-3048109801 to P.M.H.) and by the National Science Foundation-supported National Center for Supercomputing Applications Blue Waters Graduate Research Fellowship Program (under Grant No. 0725070, subaward 15836, to P.M.H.). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation

Phylogenomics Reveals Ancient Gene Tree Discordance in the Amphibian Tree of Life

Molecular phylogenies have yielded strong support for many parts of the amphibian Tree of Life, but poor support for the resolution of deeper nodes, including relationships among families and orders. To clarify these relationships, we provide a phylogenomic perspective on amphibian relationships by developing a taxon-specific Anchored Hybrid Enrichment protocol targeting hundreds of conserved exons which are effective across the class. After obtaining data from 220 loci for 286 species (representing 94% of the families and 44% of the genera), we estimate a phylogeny for extant amphibians and identify gene tree–species tree conflict across the deepest branches of the amphibian phylogeny. We perform locus-by-locus genealogical interrogation of alternative topological hypotheses for amphibian monophyly, focusing on interordinal relationships. We find that phylogenetic signal deep in the amphibian phylogeny varies greatly across loci in a manner that is consistent with incomplete lineage sorting in the ancestral lineage of extant amphibians. Our results overwhelmingly support amphibian monophyly and a sister relationship between frogs and salamanders, consistent with the Batrachia hypothesis. Species tree analyses converge on a small set of topological hypotheses for the relationships among extant amphibian families. These results clarify several contentious portions of the amphibian Tree of Life, which in conjunction with a set of vetted fossil calibrations, support a surprisingly younger timescale for crown and ordinal amphibian diversification than previously reported. More broadly, our study provides insight into the sources, magnitudes, and heterogeneity of support across loci in phylogenomic data sets