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      Tracking temporal shifts in area, biomes, and pollinators in the radiation of Salvia (sages) across continents: leveraging anchored hybrid enrichment and targeted sequence data

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          Abstract

          Premise of the Study

          A key question in evolutionary biology is why some clades are more successful by being widespread geographically, biome diverse, or species‐rich. To extend understanding of how shifts in area, biomes, and pollinators impact diversification in plants, we examined the relationships of these shifts to diversification across the mega‐genus Salvia.

          Methods

          A chronogram was developed from a supermatrix of anchored hybrid enrichment genomic data and targeted sequence data for over 500 of the nearly 1000 Salvia species. Ancestral areas and biomes were reconstructed using BioGeo BEARS. Pollinator guilds were scored, ancestral pollinators determined, shifts in pollinator guilds identified, and rates of pollinator switches compared.

          Key Results

          A well‐resolved phylogenetic backbone of Salvia and updated subgeneric designations are presented. Salvia originated in Southwest Asia in the Oligocene and subsequently dispersed worldwide. Biome shifts are frequent from a likely ancestral lineage utilizing broadleaf and/or coniferous forests and/or arid shrublands. None of the four species diversification shifts are correlated to shifts in biomes. Shifts in pollination system are not correlated to species diversification shifts, except for one hummingbird shift that precedes a major shift in diversification near the crown of New World subgen. Calosphace. Multiple reversals back to bee pollination occurred within this hummingbird clade.

          Conclusions

          Salvia diversified extensively in different continents, biomes, and with both bee and bird pollinators. The lack of tight correlation of area, biome, and most pollinator shifts to the four documented species diversification shifts points to other important drivers of speciation in Salvia.

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          Most cited references130

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          Trends, rhythms, and aberrations in global climate 65 Ma to present.

          Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.
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            Ecology and the origin of species.

            The ecological hypothesis of speciation is that reproductive isolation evolves ultimately as a consequence of divergent natural selection on traits between environments. Ecological speciation is general and might occur in allopatry or sympatry, involve many agents of natural selection, and result from a combination of adaptive processes. The main difficulty of the ecological hypothesis has been the scarcity of examples from nature, but several potential cases have recently emerged. I review the mechanisms that give rise to new species by divergent selection, compare ecological speciation with its alternatives, summarize recent tests in nature, and highlight areas requiring research.
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              Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades.

              Founder-event speciation, where a rare jump dispersal event founds a new genetically isolated lineage, has long been considered crucial by many historical biogeographers, but its importance is disputed within the vicariance school. Probabilistic modeling of geographic range evolution creates the potential to test different biogeographical models against data using standard statistical model choice procedures, as long as multiple models are available. I re-implement the Dispersal-Extinction-Cladogenesis (DEC) model of LAGRANGE in the R package BioGeoBEARS, and modify it to create a new model, DEC + J, which adds founder-event speciation, the importance of which is governed by a new free parameter, [Formula: see text]. The identifiability of DEC and DEC + J is tested on data sets simulated under a wide range of macroevolutionary models where geography evolves jointly with lineage birth/death events. The results confirm that DEC and DEC + J are identifiable even though these models ignore the fact that molecular phylogenies are missing many cladogenesis and extinction events. The simulations also indicate that DEC will have substantially increased errors in ancestral range estimation and parameter inference when the true model includes + J. DEC and DEC + J are compared on 13 empirical data sets drawn from studies of island clades. Likelihood-ratio tests indicate that all clades reject DEC, and AICc model weights show large to overwhelming support for DEC + J, for the first time verifying the importance of founder-event speciation in island clades via statistical model choice. Under DEC + J, ancestral nodes are usually estimated to have ranges occupying only one island, rather than the widespread ancestors often favored by DEC. These results indicate that the assumptions of historical biogeography models can have large impacts on inference and require testing and comparison with statistical methods. © The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
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                Author and article information

                Contributors
                kjsytsma@wisc.edu
                Journal
                Am J Bot
                Am. J. Bot
                10.1002/(ISSN)1537-2197
                AJB2
                American Journal of Botany
                John Wiley and Sons Inc. (Hoboken )
                0002-9122
                1537-2197
                15 April 2019
                April 2019
                : 106
                : 4 ( doiID: 10.1002/ajb2.2019.106.issue-4 )
                : 573-597
                Affiliations
                [ 1 ] Department of Botany University of Wisconsin‐Madison Madison WI 53706 USA
                [ 2 ] Department of Biology University of Nebraska at Kearney Kearney NE 68849 USA
                [ 3 ] CONACYT Instituto Politécnico Nacional CIIDIR ‐ Durango Durango C.P. 34234 Mexico
                [ 4 ] Mehmet Akif Ersoy mah. 269. cad. Urankent Prestij Konutları C16 Blok, No. 53 Demetevler Ankara Turkey
                [ 5 ] Research Laboratory of Ecology and Environment Department of Environment Biological Sciences Faculty of Nature and Life Sciences Université de Bejaia Targa Ouzemmour 06000 Bejaia Algeria
                [ 6 ] Key Laboratory for Plant Diversity and Biogeography of East Asia Kunming Institute of Botany Chinese Academy of Sciences Kunming Yunnan 650201 China
                [ 7 ] College of Life Sciences Guizhou University Guiyang 550025 Guizhou China
                [ 8 ] Union High School 6636 S. Mingo Road Tulsa OK 74133 USA
                [ 9 ] Department of Biological Science Florida State University Tallahassee FL 32306 USA
                [ 10 ] Department of Scientific Computing Florida State University Tallahassee FL 32306 USA
                Author notes
                [*] [* ]Author for correspondence (e‐mail: kjsytsma@ 123456wisc.edu )
                Article
                AJB21268
                10.1002/ajb2.1268
                6850103
                30986330
                c7a84a6c-b4d3-4d82-93b9-0ef03b5784b1
                © 2019 The Authors. American Journal of Botany is published by Wiley Periodicals, Inc. on behalf of the Botanical Society of America.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 04 September 2018
                : 31 January 2019
                Page count
                Figures: 9, Tables: 3, Pages: 25, Words: 21509
                Funding
                Funded by: NSF‐DEB , open-funder-registry 10.13039/100000001;
                Award ID: DEB‐1046355
                Award ID: DEB‐1655606
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                April 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:12.11.2019

                adaptive radiation,biogeobears,evolution,historical biogeography,hummingbird,lamiaceae,long‐distance dispersal,niche,phylogenomics,species diversification

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