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Mitochondrial phylogeography of the ponderosa pines: widespread gene capture, interspecific sharing, and two unique lineages

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Abstract

The mitochondrial phylogeography of some conifers shows evidence of introgression from sympatric congeners, with mitochondrial lineages not always reflecting species. This suggests that unique mitochondrial haplotypes previously reported in the ponderosa pines (Pinus subsection Ponderosae) from the USA might be more widespread in taxa not yet sampled. Recent nuclear and plastome phylogenies placed Pinus ponderosa paraphyletic in relation to Ponderosae in Mexico and Central America and confirmed that sympatric Pinus jeffreyi is more closely related to the California big-cone pines (Pinus subsection Sabinianae). We describe a broad survey of the repeated motifs in nad1 intron 2 of Ponderosae and Sabinianae, which revealed that most of the 27 mitochondrial haplotypes were not exclusive to a taxon but showed strong geographic patterns. In surprising contrast to nuclear and plastid phylogenies that resolve a monophyletic P. jeffreyi, unidirectional mitochondrial capture by P. jeffreyi (Sabinianae) from P. ponderosa was observed in all 28 samples of Jeffrey pine. Confirming the paraphyly of P. ponderosa sensu lato, mitochondrial haplotypes found mostly west and those found mostly east of the Great Basin each have more similarity to haplotypes found in Mexican taxa than they have to each other. Two distinctive haplotypes that were terminal nodes on the network were confirmed to be endemic to the Great Basin, USA, suggesting that they arose in place and have been maintained in isolation. Altogether, our results indicate a history of complex and intriguing mitochondrial relationships among the ponderosa pine species, especially between P. ponderosa and P. jeffreyi.

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Acknowledgements

We thank Jean Bousquet, David Charlet, George Ferguson, Valerie Hipkins, Stephen K. Langer, Robert Latta, Sergio Hernández León, Aaron Liston, Diana Ramos Dorantes, Charles S. Rand, and anonymous reviewers for their comments on earlier versions of the manuscript. Hendrix College students Adam Bigott, Hassan Karemera, Nicole Segear, Mason Sifford, and Austin Wofford contributed to the laboratory and analytical work on these mitochondrial data as part of their undergraduate research projects. Other Hendrix students helped with field collections and DNA isolations: Blake Cooper, Connor Douglas, Kristen Finch, Jack Finney, Payton Lea, Julia Lefler, Brandon Linz, Samuel Lockhart, Trang Nguyen, Dakota Pouncey, Brian Schumacher, Mason Sifford, Joshua Smith, Kevin Spatz, and Pete Wills. Land managers who protect these populations and permitted our collections are gratefully acknowledged: Bighorn, Black Hills, Cleveland, Colville, Coronado, Deschutes, Eldorado, Fremont-Winema, Humboldt-Toiyabe, Inyo, Kaibab, Klamath, Los Padres, Mendocino, Modoc, Nez Perce, Ochoco, San Bernardino, San Juan, Santa Fe, Sequoia, Shasta-Trinity, Sierra, Six Rivers, Umpqua, and Wasatch National Forests; California State Parks (Henry Coe and Henry Cowell), Fred Lawrence Whipple Observatory, Guadalupe National Park, Hualapai Mountain Park (Mohave County, AZ), Joint Base Lewis-McChord, North Sierra Tree Improvement Association, Sierra Pacific Industries, Quail Hollow Park (Santa Cruz County, CA), the Nature Conservancy, University of California Santa Cruz Arboretum, and University of California Reserves (Landel-Hills Big Creek and James San Jacinto).

Funding

A. W. and her students received support from Arkansas SURF, Arkansas Academy of Science Undergraduate Research Fund, and the Hendrix College Odyssey program; K. M. P. was funded with Cost Share Agreement 18-CS-11330110–026 between the U.S. Department of Agriculture, Forest Service, Southern Research Station, and North Carolina State University; D. S. G. was funded from Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (DGAPA PAPIIT-IN228209).

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Authors and Affiliations

  1. Biology Department, Hendrix College, Retired, 1600 Washington Ave, Conway, AR, USA

    Ann Willyard

  2. Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México, 04510, Mexico City, Mexico

    David S. Gernandt & Alejandro López-Reyes

  3. Department of Forestry and Environmental Resources, North Carolina State University, Research Triangle Park, Raleigh, NC, 27709, USA

    Kevin M. Potter

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Contributions

A. W. designed the experiment, collected plant samples, supervised student lab work, aligned the nucleotide sequences, and wrote the manuscript; D. S. G. collected plant samples, supervised lab work, and contributed to the manuscript; A. L. R. collected plant samples, sequenced nucleotides, and contributed to the manuscript; K. M. P. advised experimental design and contributed to the manuscript.

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Correspondence to Ann Willyard.

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Data archiving statement

Nucleotide sequences were submitted to GenBank (MK766513–MK766718). Three Supplemental Data files were included with this article. Online Resource 3 lists the geographic location and observed haplotypes for 206 individuals of 22 taxa from 123 locations in the USA, Mexico, and Guatemala. The 11 GenBank accessions that were used are included in the table without geographic location. Online Resource 4 is the alignment of 217 samples, with motif numbers 1–8 (Fig. 2) inserted before each motif to aid alignment and Online Resource 5 is the alignment without motif columns. The first characters of each sample name in the alignments give the haplotype. Online Resource 6 is the binary matrix based on the presence/absence of each motif repeat that was used to create the median joining network.

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Willyard, A., Gernandt, D.S., López-Reyes, A. et al. Mitochondrial phylogeography of the ponderosa pines: widespread gene capture, interspecific sharing, and two unique lineages. Tree Genetics & Genomes 17, 47 (2021). https://doi.org/10.1007/s11295-021-01529-4

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  • DOI: https://doi.org/10.1007/s11295-021-01529-4

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