Title: Extensive Phylogenomic Discordance and the Complex Evolutionary History of the Neotropical Cat Genus Leopardus
Abstract Even in the genomics era, the phylogeny of Neotropical small felids comprised in the genus Leopardus remains contentious. We used whole-genome resequencing data to construct a time-calibrated consensus phylogeny of this group, quantify phylogenomic discordance, test for interspecies introgression, and assess patterns of genetic diversity and demographic history. We infer that the Leopardus radiation started in the Early Pliocene as an initial speciation burst, followed by another in its subgenus Oncifelis during the Early Pleistocene. Our findings challenge the long-held notion that ocelot (Leopardus pardalis) and margay (L. wiedii) are sister species and instead indicate that margay is most closely related to the enigmatic Andean cat (L. jacobita), whose whole-genome data are reported here for the first time. In addition, we found that the newly sampled Andean tiger cat (L. tigrinus pardinoides) population from Colombia associates closely with Central American tiger cats (L. tigrinus oncilla). Genealogical discordance was largely attributable to incomplete lineage sorting, yet was augmented by strong gene flow between ocelot and the ancestral branch of Oncifelis, as well as between Geoffroy's cat (L. geoffroyi) and southern tiger cat (L. guttulus). Contrasting demographic trajectories have led to disparate levels of current genomic diversity, with a nearly tenfold difference in heterozygosity between Andean cat and ocelot, spanning the entire range of variability found in extant felids. Our analyses improved our understanding of the speciation history and diversity patterns in this felid radiation, and highlight the benefits to phylogenomic inference of embracing the many heterogeneous signals scattered across the genome. more »« less
Abstract A rapid proliferation in the availability of whole genome sequences (WGS), often with relatively low read depth, offers an unprecedented opportunity for phylogenomic advances using publicly available data, but there are several key challenges in applying these data. Using low‐coverage WGS data for the ant species ofFormica, we conducted detailed comparisons on two different analytical pipelines (reference‐based vs. de novo genome assembly), four types of datasets (5‐kbp‐window, ultra‐conserved element [UCE], single‐copy ortholog [BUSCO] and mitogenome), and a series of analytical procedures (e.g. concatenation vs. coalescent analyses) to identify which are robust to typical WGS data. The results show that at a shallow scale of phylogenetic relationships of closely related species 5‐kbp‐windows from the reference‐based pipeline and UCEs from the de novo assemblies are more successful than the BUSCOs in recovering informative markers for phylogenetic inference. Compared with concatenation analyses, coalescent analyses often resulted in disparate deeper relationships in the phylogeny. This study also uncovers evident mito‐nuclear discordance and demonstrates genome‐wide gene conflicts in phylogenetic signals, both pointing to possible incomplete lineage sorting and/or hybridization during the early, rapid radiation ofFormicaants. Divergence dating analyses show that different types of data and analytical methods could result in inconsistent time estimates, highlighting the potential need for multiple approaches to better understand species divergence. The strengths and weaknesses of different analytical pipelines and strategies are discussed. Findings from this study provide valuable insights for large‐scale phylogenomic projects using WGS data.
Mirarab, Siavash; Rivas-González, Iker; Feng, Shaohong; Stiller, Josefin; Fang, Qi; Mai, Uyen; Hickey, Glenn; Chen, Guangji; Brajuka, Nadolina; Fedrigo, Olivier; et al
(, Proceedings of the National Academy of Sciences)
Genomes are typically mosaics of regions with different evolutionary histories. When speciation events are closely spaced in time, recombination makes the regions sharing the same history small, and the evolutionary history changes rapidly as we move along the genome. When examining rapid radiations such as the early diversification of Neoaves 66 Mya, typically no consistent history is observed across segments exceeding kilobases of the genome. Here, we report an exception. We found that a 21-Mb region in avian genomes, mapped to chicken chromosome 4, shows an extremely strong and discordance-free signal for a history different from that of the inferred species tree. Such a strong discordance-free signal, indicative of suppressed recombination across many millions of base pairs, is not observed elsewhere in the genome for any deep avian relationships. Although long regions with suppressed recombination have been documented in recently diverged species, our results pertain to relationships dating circa 65 Mya. We provide evidence that this strong signal may be due to an ancient rearrangement that blocked recombination and remained polymorphic for several million years prior to fixation. We show that the presence of this region has misled previous phylogenomic efforts with lower taxon sampling, showing the interplay between taxon and locus sampling. We predict that similar ancient rearrangements may confound phylogenetic analyses in other clades, pointing to a need for new analytical models that incorporate the possibility of such events.
Abstract A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents—a large and ecologically diverse group that gave rise to the laboratory mouse and rat model systems. Combining recently published linked-read genome assemblies for seven murine species with other available rodent genomes, we first used ultraconserved elements (UCEs) to infer a robust time-calibrated species tree. We then used whole genomes to examine finer-scale patterns of discordance across ∼12 million years of divergence. We found that proximate chromosomal regions tended to have more similar phylogenetic histories. There was no clear relationship between local tree similarity and recombination rates in house mice, but we did observe a correlation between recombination rates and average similarity to the species tree. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to appreciably less discordance. Finally, we show that assuming a single species tree can result in substantial deviation from the results with gene trees when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.
Sarver, Brice A; Herrera, Nathanael D; Sneddon, David; Hunter, Samuel S; Settles, Matthew L; Kronenberg, Zev; Demboski, John R; Good, Jeffrey M; Sullivan, Jack
(, Systematic Biology)
Kubatko, Laura
(Ed.)
Abstract Evidence from natural systems suggests that hybridization between animal species is more common than traditionally thought, but the overall contribution of introgression to standing genetic variation within species remains unclear for most animal systems. Here, we use targeted exon capture to sequence thousands of nuclear loci and complete mitochondrial genomes from closely related chipmunk species in the Tamias quadrivittatus group that are distributed across the Great Basin and the central and southern Rocky Mountains of North America. This recent radiation includes six overlapping, ecologically distinct species (Tamias canipes, Tamias cinereicollis, Tamias dorsalis, T. quadrivittatus, Tamias rufus, and Tamias umbrinus) that show evidence for widespread introgression across species boundaries. Such evidence has historically been derived from a handful of markers, typically focused on mitochondrial loci, to describe patterns of introgression; consequently, the extent of introgression of nuclear genes is less well characterized. We conducted a series of phylogenomic and species-tree analyses to resolve the phylogeny of six species in this group. In addition, we performed several population-genomic analyses to characterize nuclear genomes and infer coancestry among individuals. Furthermore, we used emerging quartets-based approaches to simultaneously infer the species tree (SVDquartets) and identify introgression (HyDe). We found that, in spite of rampant introgression of mitochondrial genomes between some species pairs (and sometimes involving up to three species), there appears to be little to no evidence for nuclear introgression. These findings mirror other genomic results where complete mitochondrial capture has occurred between chipmunk species in the absence of appreciable nuclear gene flow. The underlying causes of recurrent massive cytonuclear discordance remain unresolved in this group but mitochondrial DNA appears highly misleading of population histories as a whole. Collectively, it appears that chipmunk species boundaries are largely impermeable to nuclear gene flow and that hybridization, while pervasive with respect to mtDNA, has likely played a relatively minor role in the evolutionary history of this group. [Cytonuclear discordance; hyridization; introgression, phylogenomics; SVDquartets; Tamias.]
Foley, Nicole M.; Mason, Victor C.; Harris, Andrew J.; Bredemeyer, Kevin R.; Damas, Joana; Lewin, Harris A.; Eizirik, Eduardo; Gatesy, John; Karlsson, Elinor K.; Lindblad-Toh, Kerstin; et al
(, Science)
INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
Lescroart, Jonas, Bonilla-Sánchez, Alejandra, Napolitano, Constanza, Buitrago-Torres, Diana L., Ramírez-Chaves, Héctor E., Pulido-Santacruz, Paola, Murphy, William J., Svardal, Hannes, Eizirik, Eduardo, and O'Connell, ed., Mary. Extensive Phylogenomic Discordance and the Complex Evolutionary History of the Neotropical Cat Genus Leopardus. Molecular Biology and Evolution 40.12 Web. doi:10.1093/molbev/msad255.
Lescroart, Jonas, Bonilla-Sánchez, Alejandra, Napolitano, Constanza, Buitrago-Torres, Diana L., Ramírez-Chaves, Héctor E., Pulido-Santacruz, Paola, Murphy, William J., Svardal, Hannes, Eizirik, Eduardo, and O'Connell, ed., Mary.
"Extensive Phylogenomic Discordance and the Complex Evolutionary History of the Neotropical Cat Genus Leopardus". Molecular Biology and Evolution 40 (12). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1093/molbev/msad255.https://par.nsf.gov/biblio/10478338.
@article{osti_10478338,
place = {Country unknown/Code not available},
title = {Extensive Phylogenomic Discordance and the Complex Evolutionary History of the Neotropical Cat Genus Leopardus},
url = {https://par.nsf.gov/biblio/10478338},
DOI = {10.1093/molbev/msad255},
abstractNote = {Abstract Even in the genomics era, the phylogeny of Neotropical small felids comprised in the genus Leopardus remains contentious. We used whole-genome resequencing data to construct a time-calibrated consensus phylogeny of this group, quantify phylogenomic discordance, test for interspecies introgression, and assess patterns of genetic diversity and demographic history. We infer that the Leopardus radiation started in the Early Pliocene as an initial speciation burst, followed by another in its subgenus Oncifelis during the Early Pleistocene. Our findings challenge the long-held notion that ocelot (Leopardus pardalis) and margay (L. wiedii) are sister species and instead indicate that margay is most closely related to the enigmatic Andean cat (L. jacobita), whose whole-genome data are reported here for the first time. In addition, we found that the newly sampled Andean tiger cat (L. tigrinus pardinoides) population from Colombia associates closely with Central American tiger cats (L. tigrinus oncilla). Genealogical discordance was largely attributable to incomplete lineage sorting, yet was augmented by strong gene flow between ocelot and the ancestral branch of Oncifelis, as well as between Geoffroy's cat (L. geoffroyi) and southern tiger cat (L. guttulus). Contrasting demographic trajectories have led to disparate levels of current genomic diversity, with a nearly tenfold difference in heterozygosity between Andean cat and ocelot, spanning the entire range of variability found in extant felids. Our analyses improved our understanding of the speciation history and diversity patterns in this felid radiation, and highlight the benefits to phylogenomic inference of embracing the many heterogeneous signals scattered across the genome.},
journal = {Molecular Biology and Evolution},
volume = {40},
number = {12},
publisher = {Oxford University Press},
author = {Lescroart, Jonas and Bonilla-Sánchez, Alejandra and Napolitano, Constanza and Buitrago-Torres, Diana L. and Ramírez-Chaves, Héctor E. and Pulido-Santacruz, Paola and Murphy, William J. and Svardal, Hannes and Eizirik, Eduardo and O'Connell, ed., Mary},
}
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