Title: Earth history and the passerine superradiation
Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation. more »« less
Zenil-Ferguson, Rosana; McEntee, Jay P; Burleigh, J Gordon; Duckworth, Renée A
(, Systematic Biology)
Ruane, Sara
(Ed.)
Abstract A long-standing hypothesis in evolutionary biology is that the evolution of resource specialization can lead to an evolutionary dead end, where specialists have low diversification rates and limited ability to evolve into generalists. In recent years, advances in comparative methods investigating trait-based differences associated with diversification have enabled more robust tests of this idea and have found mixed support. We test the evolutionary dead end hypothesis by estimating net diversification rate differences associated with nest-type specialization among 3224 species of passerine birds. In particular, we test whether the adoption of hole-nesting, a nest-type specialization that decreases predation, results in reduced diversification rates relative to nesting outside of holes. Further, we examine whether evolutionary transitions to the specialist hole-nesting state have been more frequent than transitions out of hole-nesting. Using diversification models that accounted for background rate heterogeneity and different extinction rate scenarios, we found that hole-nesting specialization was not associated with diversification rate differences. Furthermore, contrary to the assumption that specialists rarely evolve into generalists, we found that transitions out of hole-nesting occur more frequently than transitions into hole-nesting. These results suggest that interspecific competition may limit adoption of hole-nesting, but that such competition does not result in limited diversification of hole-nesters. In conjunction with other recent studies using robust comparative methods, our results add to growing evidence that evolutionary dead ends are not a typical outcome of resource specialization. [Cavity nesting; diversification; hidden-state models; passerines; resource specialization.]
Abstract Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.
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.
Finger, Nicholas; Farleigh, Keaka; Bracken, Jason T; Leaché, Adam D; François, Olivier; Yang, Ziheng; Flouri, Tomas; Charran, Tristan; Jezkova, Tereza; Williams, Dean A; et al
(, Genome Biology and Evolution)
Baldauf, Sandra
(Ed.)
Abstract The southwestern and central United States serve as an ideal region to test alternative hypotheses regarding biotic diversification. Genomic data can now be combined with sophisticated computational models to quantify the impacts of paleoclimate change, geographic features, and habitat heterogeneity on spatial patterns of genetic diversity. In this study, we combine thousands of genotyping-by-sequencing (GBS) loci with mtDNA sequences (ND1) from the Texas horned lizard (Phrynosoma cornutum) to quantify relative support for different catalysts of diversification. Phylogenetic and clustering analyses of the GBS data indicate support for at least three primary populations. The spatial distribution of populations appears concordant with habitat type, with desert populations in AZ and NM showing the largest genetic divergence from the remaining populations. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype–environment association with bioclimatic variables supports divergence along precipitation gradients more than along temperature gradients. Demographic analyses support a complex history, with introgression and gene flow playing an important role during diversification. Bayesian multispecies coalescent analyses with introgression (MSci) analyses also suggest that gene flow occurred between populations. Paleo-species distribution models support two southern refugia that geographically correspond to contemporary lineages. We find that divergence times are underestimated and population sizes are overestimated when introgression occurred and is ignored in coalescent analyses, and furthermore, inference of ancient introgression events and demographic history is sensitive to inclusion of a single recently admixed sample. Our analyses cannot refute the riverine barrier or glacial refugia hypotheses. Results also suggest that populations are continuing to diverge along habitat gradients. Finally, the strong evidence of admixture, gene flow, and mtDNA introgression among populations suggests that P. cornutum should be considered a single widespread species under the General Lineage Species Concept.
Loria, Stephanie F.; Prendini, Lorenzo
(, Scientific Reports)
null
(Ed.)
Abstract The ‘Out of India’ hypothesis is often invoked to explain patterns of distribution among Southeast Asian taxa. According to this hypothesis, Southeast Asian taxa originated in Gondwana, diverged from their Gondwanan relatives when the Indian subcontinent rifted from Gondwana in the Late Jurassic, and colonized Southeast Asia when it collided with Eurasia in the early Cenozoic. A growing body of evidence suggests these events were far more complex than previously understood, however. The first quantitative reconstruction of the biogeography of Asian forest scorpions (Scorpionidae Latreille, 1802: Heterometrinae Simon, 1879) is presented here. Divergence time estimation, ancestral range estimation, and diversification analyses are used to determine the origins, dispersal and diversification patterns of these scorpions, providing a timeline for their biogeographical history that can be summarized into four major events. (1) Heterometrinae diverged from other Scorpionidae on the African continent after the Indian subcontinent became separated in the Cretaceous. (2) Environmental stresses during the Cretaceous–Tertiary (KT) mass extinction caused range contraction, restricting one clade of Heterometrinae to refugia in southern India (the Western Ghats) and Sri Lanka (the Central Highlands). (3) Heterometrinae dispersed to Southeast Asia three times during India’s collision with Eurasia, the first dispersal event occurring as the Indian subcontinent brushed up against the western side of Sumatra, and the other two events occurring as India moved closer to Eurasia. (4) Indian Heterometrinae, confined to southern India and Sri Lanka during the KT mass extinction, recolonized the Deccan Plateau and northern India, diversifying into new, more arid habitats after environmental conditions stabilized. These hypotheses, which are congruent with the geological literature and biogeographical analyses of other taxa from South and Southeast Asia, contribute to an improved understanding of the dispersal and diversification patterns of taxa in this biodiverse and geologically complex region.
Oliveros, Carl H., Field, Daniel J., Ksepka, Daniel T., Barker, F. Keith, Aleixo, Alexandre, Andersen, Michael J., Alström, Per, Benz, Brett W., Braun, Edward L., Braun, Michael J., Bravo, Gustavo A., Brumfield, Robb T., Chesser, R. Terry, Claramunt, Santiago, Cracraft, Joel, Cuervo, Andrés M., Derryberry, Elizabeth P., Glenn, Travis C., Harvey, Michael G., Hosner, Peter A., Joseph, Leo, Kimball, Rebecca T., Mack, Andrew L., Miskelly, Colin M., Peterson, A. Townsend, Robbins, Mark B., Sheldon, Frederick H., Silveira, Luís Fábio, Smith, Brian Tilston, White, Noor D., Moyle, Robert G., and Faircloth, Brant C. Earth history and the passerine superradiation. Proceedings of the National Academy of Sciences 116.16 Web. doi:10.1073/pnas.1813206116.
Oliveros, Carl H., Field, Daniel J., Ksepka, Daniel T., Barker, F. Keith, Aleixo, Alexandre, Andersen, Michael J., Alström, Per, Benz, Brett W., Braun, Edward L., Braun, Michael J., Bravo, Gustavo A., Brumfield, Robb T., Chesser, R. Terry, Claramunt, Santiago, Cracraft, Joel, Cuervo, Andrés M., Derryberry, Elizabeth P., Glenn, Travis C., Harvey, Michael G., Hosner, Peter A., Joseph, Leo, Kimball, Rebecca T., Mack, Andrew L., Miskelly, Colin M., Peterson, A. Townsend, Robbins, Mark B., Sheldon, Frederick H., Silveira, Luís Fábio, Smith, Brian Tilston, White, Noor D., Moyle, Robert G., & Faircloth, Brant C. Earth history and the passerine superradiation. Proceedings of the National Academy of Sciences, 116 (16). https://doi.org/10.1073/pnas.1813206116
Oliveros, Carl H., Field, Daniel J., Ksepka, Daniel T., Barker, F. Keith, Aleixo, Alexandre, Andersen, Michael J., Alström, Per, Benz, Brett W., Braun, Edward L., Braun, Michael J., Bravo, Gustavo A., Brumfield, Robb T., Chesser, R. Terry, Claramunt, Santiago, Cracraft, Joel, Cuervo, Andrés M., Derryberry, Elizabeth P., Glenn, Travis C., Harvey, Michael G., Hosner, Peter A., Joseph, Leo, Kimball, Rebecca T., Mack, Andrew L., Miskelly, Colin M., Peterson, A. Townsend, Robbins, Mark B., Sheldon, Frederick H., Silveira, Luís Fábio, Smith, Brian Tilston, White, Noor D., Moyle, Robert G., and Faircloth, Brant C.
"Earth history and the passerine superradiation". Proceedings of the National Academy of Sciences 116 (16). Japan: Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1813206116.https://par.nsf.gov/biblio/10089764.
@article{osti_10089764,
place = {Japan},
title = {Earth history and the passerine superradiation},
url = {https://par.nsf.gov/biblio/10089764},
DOI = {10.1073/pnas.1813206116},
abstractNote = {Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.},
journal = {Proceedings of the National Academy of Sciences},
volume = {116},
number = {16},
publisher = {Proceedings of the National Academy of Sciences},
author = {Oliveros, Carl H. and Field, Daniel J. and Ksepka, Daniel T. and Barker, F. Keith and Aleixo, Alexandre and Andersen, Michael J. and Alström, Per and Benz, Brett W. and Braun, Edward L. and Braun, Michael J. and Bravo, Gustavo A. and Brumfield, Robb T. and Chesser, R. Terry and Claramunt, Santiago and Cracraft, Joel and Cuervo, Andrés M. and Derryberry, Elizabeth P. and Glenn, Travis C. and Harvey, Michael G. and Hosner, Peter A. and Joseph, Leo and Kimball, Rebecca T. and Mack, Andrew L. and Miskelly, Colin M. and Peterson, A. Townsend and Robbins, Mark B. and Sheldon, Frederick H. and Silveira, Luís Fábio and Smith, Brian Tilston and White, Noor D. and Moyle, Robert G. and Faircloth, Brant C.},
}
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