Phylogeny and Biogeography of the Carnivorous Plant Family Sarraceniaceae

PLOS ONE, Dec 2019

The carnivorous plant family Sarraceniaceae comprises three genera of wetland-inhabiting pitcher plants: Darlingtonia in the northwestern United States, Sarracenia in eastern North America, and Heliamphora in northern South America. Hypotheses concerning the biogeographic history leading to this unusual disjunct distribution are controversial, in part because genus- and species-level phylogenies have not been clearly resolved. Here, we present a robust, species-rich phylogeny of Sarraceniaceae based on seven mitochondrial, nuclear, and plastid loci, which we use to illuminate this family's phylogenetic and biogeographic history. The family and genera are monophyletic: Darlingtonia is sister to a clade consisting of Heliamphora+Sarracenia. Within Sarracenia, two clades were strongly supported: one consisting of S. purpurea, its subspecies, and S. rosea; the other consisting of nine species endemic to the southeastern United States. Divergence time estimates revealed that stem group Sarraceniaceae likely originated in South America 44–53 million years ago (Mya) (highest posterior density [HPD] estimate = 47 Mya). By 25–44 (HPD = 35) Mya, crown-group Sarraceniaceae appears to have been widespread across North and South America, and Darlingtonia (western North America) had diverged from Heliamphora+Sarracenia (eastern North America+South America). This disjunction and apparent range contraction is consistent with late Eocene cooling and aridification, which may have severed the continuity of Sarraceniaceae across much of North America. Sarracenia and Heliamphora subsequently diverged in the late Oligocene, 14–32 (HPD = 23) Mya, perhaps when direct overland continuity between North and South America became reduced. Initial diversification of South American Heliamphora began at least 8 Mya, but diversification of Sarracenia was more recent (2–7, HPD = 4 Mya); the bulk of southeastern United States Sarracenia originated co-incident with Pleistocene glaciation, <3 Mya. Overall, these results suggest climatic change at different temporal and spatial scales in part shaped the distribution and diversity of this carnivorous plant clade.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0039291&type=printable

Phylogeny and Biogeography of the Carnivorous Plant Family Sarraceniaceae

et al. (2012) Phylogeny and Biogeography of the Carnivorous Plant Family Sarraceniaceae. PLoS ONE 7(6): e39291. doi:10.1371/journal.pone.0039291 Phylogeny and Biogeography of the Carnivorous Plant Family Sarraceniaceae Aaron M. Ellison 0 Elena D. Butler 0 Emily Jean Hicks 0 Robert F. C. Naczi 0 Patrick J. Calie 0 Charles D. Bell 0 Charles C. Davis 0 Sebastien Lavergne, CNRS/Universite Joseph-Fourier, France 0 1 Harvard Forest, Harvard University , Petersham , Massachusetts, United States of America, 2 Organismic and Evolutionary Biology, Harvard University, Massachusetts, United States of America, 3 Biological Sciences, Eastern Kentucky University , Richmond , Kentucky, United States of America, 4 Regulatory Services, University of Kentucky, Lexington, Kentucky, United States of America , 5 The New York Botanical Garden, Bronx , New York, United States of America, 6 University of New Orleans , New Orleans, Louisiana , United States of America The carnivorous plant family Sarraceniaceae comprises three genera of wetland-inhabiting pitcher plants: Darlingtonia in the northwestern United States, Sarracenia in eastern North America, and Heliamphora in northern South America. Hypotheses concerning the biogeographic history leading to this unusual disjunct distribution are controversial, in part because genus- and species-level phylogenies have not been clearly resolved. Here, we present a robust, species-rich phylogeny of Sarraceniaceae based on seven mitochondrial, nuclear, and plastid loci, which we use to illuminate this family's phylogenetic and biogeographic history. The family and genera are monophyletic: Darlingtonia is sister to a clade consisting of Heliamphora+Sarracenia. Within Sarracenia, two clades were strongly supported: one consisting of S. purpurea, its subspecies, and S. rosea; the other consisting of nine species endemic to the southeastern United States. Divergence time estimates revealed that stem group Sarraceniaceae likely originated in South America 44-53 million years ago (Mya) (highest posterior density [HPD] estimate = 47 Mya). By 25-44 (HPD = 35) Mya, crown-group Sarraceniaceae appears to have been widespread across North and South America, and Darlingtonia (western North America) had diverged from Heliamphora+Sarracenia (eastern North America+South America). This disjunction and apparent range contraction is consistent with late Eocene cooling and aridification, which may have severed the continuity of Sarraceniaceae across much of North America. Sarracenia and Heliamphora subsequently diverged in the late Oligocene, 14-32 (HPD = 23) Mya, perhaps when direct overland continuity between North and South America became reduced. Initial diversification of South American Heliamphora began at least 8 Mya, but diversification of Sarracenia was more recent (2-7, HPD = 4 Mya); the bulk of southeastern United States Sarracenia originated co-incident with Pleistocene glaciation, ,3 Mya. Overall, these results suggest climatic change at different temporal and spatial scales in part shaped the distribution and diversity of this carnivorous plant clade. - Funding: Grant-in-Aid of Undergraduate Research from the Harvard University Herbaria; the Harvard College Research Program; NSF grants EF 04-31242 and DEB 05-41680 http://www.nsf.gov/; NSF-Kentucky EPSCoR Program, NIH/NCRR grant P20 RR16481 http://www.nih.gov/; and the L. R. Hesler Award from the University of Tennessee Department of Ecology and Evolutionary Biology. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Carnivory has evolved at least six times within the flowering plants [1,2] and is thought to be an adaption to increase the uptake of nitrogen and phosphorous in the nutrient-poor, aquatic and wetland environments where these plants grow [3,4]. The biogeographic distribution of carnivorous plants presents as intriguing a puzzle as the evolution of carnivory itself, but far more attention has been directed at understanding the evolution of carnivorous plants [2,3,5] than has been directed at understanding their biogeography. Here, we present the most fully-resolved phylogeny of the American pitcher-plant family Sarraceniaceae to date. We use these data to estimate molecular divergence times of the group and to address a long-standing debate on the biogeographic origin and the disjunct distribution of these three genera. Carnivorous plants grow on every continent except Antarctica. Some carnivorous plant families, such as the Cephalotaceae, Roridulaceae, and Byblidaceae, are endemics occurring on single (sub)continents, whereas others, such as Droseraceae and Lentibulariaceae have cosmopolitan distributions [1,2,511]. The enigmatic, disjunct distribution of the three genera of the American pitcher plants, Sarraceniaceae (Fig. 1), presents an unresolved question for botani (...truncated)


This is a preview of a remote PDF: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0039291&type=printable

Aaron M. Ellison, Elena D. Butler, Emily Jean Hicks, Robert F. C. Naczi, Patrick J. Calie, Charles D. Bell, Charles C. Davis. Phylogeny and Biogeography of the Carnivorous Plant Family Sarraceniaceae, PLOS ONE, 2012, Volume 7, Issue 6, DOI: 10.1371/journal.pone.0039291