Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis)

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Abstract

Unusual patterns of mtDNA diversity can reveal interesting aspects of a species’ biology. However, making such inferences requires discerning among the many alternative scenarios that could underlie any given mtDNA pattern. Next-generation sequencing methods provide large, multilocus data sets with increased power to resolve unusual mtDNA patterns. A mtDNA-based phylogeography of the Savannah sparrow (Passerculus sandwichensis) previously identified two sympatric, but divergent (~2%) clades within the nominate subspecies group and a third clade that consisted of birds sampled from northwest Mexico. We revisited the phylogeography of this species using a population genomic data set to resolve the processes leading to the evolution of sympatric and divergent mtDNA lineages. We identified two genetic clusters in the genomic data set corresponding to (a) the nominate subspecies group and (b) northwestern Mexico birds. Following divergence, the nominate clade maintained a large, stable population, indicating that divergent mitochondrial lineages arose within a panmictic population. Simulations based on parameter estimates from this model further confirmed that this demographic history could produce observed levels of mtDNA diversity. Patterns of divergent, sympatric mtDNA lineages are frequently interpreted as admixture of historically isolated lineages. Our analyses reject this interpretation for Savannah sparrows and underscore the need for genomic data sets to resolve the evolutionary mechanisms behind anomalous, locus-specific patterns.

Original languageEnglish
Pages (from-to)1765-1783
Number of pages19
JournalMolecular Ecology
Volume28
Issue number7
DOIs
StatePublished - Apr 2019

Funding

We thank the following museums and individuals for providing tissue samples for this study: J. Cracraft, P. Sweet, & T. Trombone (AMNH); K. Bostwick (CUMV); D. Dittmann & F. Sheldon (LSUMZ); C. Witt & A. Johnson (MSB); C. Cicero & R. Bowie (MVZ); J. Rising, R. Zink & M. Westberg (ROM & BELL); P. Unitt & K. Burns (SDNHM & SDSU Museum of Biodiversity); K. Winker (UAM); C. Gebhard, & H. James (USNM); S. Birks (UWBM); K. Zyskowski (YPM). Adolfo Navarro-Siqüenza was instrumental in providing necessary permits and assistance with field logistics for work in Mexico. We also thank J. Bates, S. Hackett, B. Marks, D. Brinkmeier, J. Maley, J. McCormack and A. Gordillo Martínez for their assistance with permits and field logistics. S. M. Robles Bello, A. Hernández Cardona, D. Levey and D. Senner provided excellent field assistance in collecting samples. J. Jones and A. Hernandez helped with sequencing and laboratory work. Personnel at CDFW, IDNR and USFWS assisted with access to federal and state lands. Finally, we thank N. Sly, M. Stager, C. Wolf, R. Schweizer, J. Velotta, N. Senner, E. Beckman, the AEGG discussion group at the University of Montana, Irby Lovette, Bryan Carstens, Brian Smith and two anonymous reviewers for useful comments on the manuscript. Funding for field work and sequencing was provided by AMNH Frank M. Chapman Memorial Fund, SSE Rosemary Grant Award, SICB GIAR, Sigma-XI GIAR, UIUC Animal Biology departmental grants, Illinois Ornithological Society, Systematics Research Fund, AOU research award, Center for Latin America & Caribbean Studies Tinker Fellowship, and start-up funds to ZAC from UM and UIUC. We thank the following museums and individuals for providing tis‐ sue samples for this study: J. Cracraft, P. Sweet, & T. Trombone (AMNH); K. Bostwick (CUMV); D. Dittmann & F. Sheldon (LSUMZ); C. Witt & A. Johnson (MSB); C. Cicero & R. Bowie (MVZ); J. Rising, R. Zink & M. Westberg (ROM & BELL); P. Unitt & K. Burns (SDNHM & SDSU Museum of Biodiversity); K. Winker (UAM); C. Gebhard, & H. James (USNM); S. Birks (UWBM); K. Zyskowski (YPM). Adolfo Navarro‐Siqüenza was instrumental in providing necessary permits and assistance with field logistics for work in Mexico. We also thank J. Bates, S. Hackett, B. Marks, D. Brinkmeier, J. Maley, J. McCormack and A. Gordillo Martínez for their assistance with permits and field logistics. S. M. Robles Bello, A. Hernández Cardona, D. Levey and D. Senner provided excellent field assistance in collecting samples. J. Jones and A. Hernandez helped with sequencing and laboratory work. Personnel at CDFW, IDNR and USFWS assisted with access to federal and state lands. Finally, we thank N. Sly, M. Stager, C. Wolf, R. Schweizer, J. Velotta, N. Senner, E. Beckman, the AEGG discussion group at the University of Montana, Irby Lovette, Bryan Carstens, Brian Smith and two anonymous reviewers for useful comments on the manuscript. Funding for field work and sequencing was provided by AMNH Frank M. Chapman Memorial Fund, SSE Rosemary Grant Award, SICB GIAR, Sigma‐XI GIAR, UIUC Animal Biology departmen‐ tal grants, Illinois Ornithological Society, Systematics Research Fund, AOU research award, Center for Latin America & Caribbean Studies Tinker Fellowship, and start‐up funds to ZAC from UM and UIUC. University of Montana, Grant/Award Number: internal funds; Sigma Xi, Grant/ Award Number: Grant‐in‐aid‐of‐research; University of Illinois, Grant/Award Number: various; American Museum of Natural History, Grant/Award Number: Frank M. Chapman Memorial Fund; Systematics Association, Grant/Award Number: Systematic Research Fund; Society for the Study of Evolution, Grant/Award Number: Rosemary Grant Award; Illinois Ornithological Society, Grant/Award Number: Student research award; Society for Integrative and Comparative Biology, Grant/Award Number: Grant‐in‐aid‐of‐ research; American Ornithologists' Union, Grant/Award Number: student research award

Funders
University of Illinois at Urbana-Champaign
American Museum of Natural History
American Ornithologists' Union

    Keywords

    • Passerculus
    • Passerellidae
    • genotyping-by-sequencing
    • mitochondrial DNA
    • phylogeography

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