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Relationships among North American deer based on mitochondrial DNA and ultraconserved elements, with comments on mito-nuclear discordance

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Abstract

Despite their economic, cultural, and ecological significance, the phylogenetic relationships among North American deer remain uncertain, due in part to discordance between phylogenies built from mitochondrial DNA (mtDNA) and nuclear markers. Nuclear markers resolve mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) as reciprocally monophyletic, but mtDNA results in a mixed topology. These two genomic regions have heretofore been analyzed in isolation. We compared phylogenies built from mtDNA cytochrome b and single-nucleotide polymorphisms (SNPs) from the mitogenome and nuclear (ultraconserved elements, UCEs) markers from the same individuals to investigate mito-nuclear discordance within and between taxa in the genus Odocoileus. A Cyt b tree shows haplotype sharing between O. hemionus and O. virginianus. Mitochondrial DNA SNPs separated only O. hemionus and O. virginianus, whereas nuclear SNPs separated O. hemionus, O. virginianus, and the distinct subspecies Coues deer (O. v. couesi), Key deer (O. v. clavium), and Sitka black-tailed deer (O. h. sitkensis) plus Columbian black-tailed deer (O. h. columbianus). We found less support for O. h. columbianus as a distinct taxon, which had signs of introgression with nominate O. h. hemionus. The well-established paraphyly of mtDNA haplotypes from O. virginianus and O. hemionus is confirmed with comparisons of mtDNA and nuclear-encoded SNPs from the same individuals. Our attempts to explain mito-nuclear discordance among Odocoileus deer remain inconclusive. We suspect incomplete lineage sorting of a recent evolutionary split may explain this pattern, although mtDNA capture via ancient hybridization is also a possibility. Niche models suggested allopatric refugia at the Last Glacial Maximum for these taxa except for a parapatric or sympatric distribution estimated for O. virginianus and O. v. clavium and O. hemionus and O. h. columbianus, the latter of which might explain the modern hybrid zone.

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Data availability

Data are in GenBank and will be deposited in Dryad (UCE).

Code availability

All code and corresponding data used to produce presented results are available in the article and Online Resources.

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Acknowledgements

We received tissues from hunter-harvested deer in Nebraska via the Nebraska Game and Parks Commission, thanks to K. Decker, T. Nordeen, and J. J. Lusk. We received tissue loans from L. Olson (University of Alaska-Fairbanks), J. Heffelfinger (Arizona Game and Fish Department), and K. Watts (Florida Keys National Wildlife Refuge). We thank B. Buchanan, M. Girard, and M. Olson for lab assistance.

Funding

Nebraska Game and Parks Commission (w-113-r), Pope and Young Club (no grant number).

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Authors and Affiliations

  1. Department of Natural Science, Peru State College, Peru, NE, 68421, USA

    Lukas B. Klicka

  2. Department of Evolution, Ecology, and Organismal Biology, University of California, Riverside, 92521, USA

    Nadje Najar

  3. Departamento de Zoología, Instituto de Biología, Colección Nacional de Aves, Universidad NacionalAutónoma de México, C.P. 04510, Ciudad de Mexico, Mexico

    Hernan Vázquez-Miranda

  4. School of Natural Resources, School of Biological Sciences and Nebraska State Museum, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Robert M. Zink

Authors
  1. Lukas B. Klicka
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  2. Nadje Najar
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  4. Robert M. Zink
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Contributions

Conceptualization: HV-M and RMZ; data curation: LBK; formal analysis: LBK, NN, and RMZ; funding acquisition: RMZ; investigation: LBK, RMZ, and HV-M; methodology: LBK and HV-M; project administration: RMZ; resources: RMZ; software: LBK; supervision: RMZ; validation: LBK, RMZ, and HV-M; visualization: HV-M, writing—original draft preparation: RMZ; writing—review and editing: LBK, NN, RMZ, and HV-M.

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Correspondence to Robert M. Zink.

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Communicated by Magdalena Niedziałkowska

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Appendix

Appendix

Specimens and GenBank identifiers for Cyt b data (see also Gutierrez et al. 2017). OH = Odocoileus hemionus, OV = O. virginianus. Subspecies identifiers given if also in provided in GenBank (although taxonomy not verified). Geographic identifiers given if listed with GenBank entry. OH and OV from Nebraska are given in GenBank MN 390611–390813 and came from the following counties (OH: Arthur, Blaine, Boone, Box Butte, Brown, Cherry, Cheyenne, Custer, Dawes, Dawson, Dundy, Frontier, Furnas, Garden, Gosper, Grant, Greeley, Hayes, Hitchcock, Hold, Keith, Keya Paha, Kimball, Loup, Morrill, Red Willow, Scotts Bluff, Sheridan; OV: Otoe, York, Seward, Johnson, Pawnee, Richardson, Cass, Box Butte, Dawes, Cherry, Howard, Hall, Custer, Buffalo, Franklin, Kearney, Harlan, Garden, Valley, Loup; (Chemung Co.) and Minnesota (Washington Co.).

AF091630_OH; AY607035_OV; DQ379370_OV; DQ673136_OV; FJ188717_OH_AB; FJ188718_OH_AB; FJ188719_OH_AB; FJ188720_OH_AB; FJ188721_OH_AB; FJ188722_OH_AB; FJ188723_OH_AB; FJ188724_OH_AB; FJ188725_OH_AB; FJ188726_OH_AB_OR; FJ188727_OH_sitkensis_AK; FJ188728_OH_sitkensis_AK; FJ188729_OH_crooki_AZ; FJ188730_OH_crooki_AZ; FJ188731_OH_crooki_AZ; FJ188732_OH_crooki_AZ; FJ188733_OH_crooki_AZ; FJ188734_OH_crooki_AZ; FJ188735_OH_crooki_AZ; FJ188736_OH_crooki_AZ; FJ188737_OH_crooki_AZ; FJ188738_OH_crooki_AZ; FJ188739_OH_crooki_AZ; FJ188740_OH_crooki_AZ; FJ188741_OH_crooki_AZ; FJ188742_OH_hemionus_AZ; FJ188743_OH_hemionus_AZ; FJ188744_OH_hemionus_AZ; FJ188745_OH_hemionus_AZ; FJ188746_OH_hemionus_AZ; FJ188747_OH_hemionus_AZ; FJ188748_OH_hemionus_AZ; FJ188749_OH_eremicus_AZ; FJ188750_OH_fuliginatus; FJ188751_OH_fuliginatus; FJ188752_OH_fuliginatus; FJ188753_OH_peninsulae; FJ188754_OH_peninsulae; FJ188755_OH_peninsulae; FJ188756_OH_peninsulae; FJ188757_OH_peninsulae; FJ188758_OH_peninsulae; FJ188759_OH_columbianus; FJ188760_OH_columbianus; FJ188761_OH_columbianus; FJ188762_OH_hemionus_BC; FJ188763_OH_hemionus_BC; FJ188764_OH_hemionus_BC; FJ188765_OH_hemionus_BC; FJ188766_OH_columbianus_BC; FJ188767_OH_hemionus_BC; FJ188768_OH_hemionus_BC; FJ188769_OH_columbianus_BC_VI; FJ188770_OH_columbianus_BC_VI; FJ188771_OH_columbianus_BC_VI; FJ188772_OH_columbianus_BC_VI; FJ188773_OH_californicus_CA; FJ188774_OH_californicus_CA; FJ188775_OH_eremicus_CA; FJ188776_OH_inyoensis_CA; FJ188777_OH_inyoensis_CA; FJ188778_OH_inyoensis_CA; FJ188779_OH_inyoensis_CA; FJ188780_OH_californicus_CA; FJ188781_OH_californicus_CA; FJ188782_OH_californicus_CA; FJ188783_OH_californicus_CA; FJ188784_OH_californicus_CA; FJ188785_OH_californicus_CA; FJ188786_OH_californicus_CA; FJ188787_OH_fuliginatus_CA; FJ188788_OH_fuliginatus_CA; FJ188789_OH_fuliginatus_CA; FJ188790_OH_fuliginatus_CA; FJ188791_OH_fuliginatus_CA; FJ188792_OH_fuliginatus_CA_; FJ188793_OH_californicus_CA; FJ188794_OH_californicus_CA; FJ188795_OH_californicus_CA; FJ188796_OH_californicus_CA; FJ188797_OH_californicus_CA; FJ188798_OH_californicus_CA; FJ188799_OH_californicus_CA; FJ188800_OH_californicus_CA; FJ188801_OH_columbianus_CA; FJ188802_OH_columbianus_CA; FJ188803_OH_columbianus_CA; FJ188804_OH_columbianus_CA; FJ188805_OH_columbianus_CA; FJ188806_OH_columbianus_CA; FJ188807_OH_columbianus_CA; FJ188808_OH_crooki; FJ188809_OH_crooki; FJ188810_OH_crooki; FJ188811_OH_crooki; FJ188812_OH_crooki; FJ188813_OH_hemionus_CO; FJ188814_OH_hemionus_CO; FJ188815_OH_hemionus_CO; FJ188816_OH_hemionus_CO; FJ188817_OH_hemionus_CO; FJ188818_OH_crooki_CU; FJ188819_OH_hemionus_ID; FJ188820_OH_hemionus_ID; FJ188821_OH_hemionus_ID; FJ188822_OH_hemionus_ID; FJ188823_OH_hemionus; FJ188824_OH_hemionus_KS; FJ188825_OH_hemionus_KS; FJ188826_OH_hemionus_KS; FJ188827_OH_hemionus_KS; FJ188828_OH_hemionus_KS; FJ188829_OH_hemionus_MT; FJ188830_OH_hemionus_MT; FJ188831_OH_hemionus_MT; FJ188832_OH_hemionus_MT7; FJ188833_OH_hemionus_MT2; FJ188834_OH_hemionus_ND2; FJ188835_OH_hemionus_ND; FJ188836_OH_hemionus_ND; FJ188837_OH_hemionus_NE; FJ188838_OH_hemionus_NE; FJ188839_OH_hemionus_NE1; FJ188840_OH_crooki_NM_02; FJ188841_OH_crooki_NM; FJ188842_OH_crooki_NM; FJ188843_OH_hemionus_NM; FJ188844_OH_hemionus_NM; FJ188845_OH_hemionus_NM; FJ188846_OH_hemionus_NM; FJ188847_OH_hemionus_NV; FJ188848_OH_hemionus_NV; FJ188849_OH_hemionus_NV; FJ188850_OH_hemionus_NV; FJ188851_OH_columbianus_OR; FJ188852_OH_columbianus_OR; FJ188853_OH_columbianus_OR; FJ188854_OH_columbianus_OR; FJ188855_OH_columbianus_OR; FJ188856_OH_hemionus_OR; FJ188857_OH_hemionus_OR; FJ188858_OH_hemionus_OR; FJ188859_OH_columbianus_OR; FJ188860_OH_columbianus_OR; FJ188861_OH_columbianus_OR; FJ188862_OH_columbianus_OR; FJ188863_OH_columbianus_OR; FJ188864_OH_columbianus_OR; FJ188865_OH_columbianus_OR; FJ188866_OH_columbianus_OR; FJ188867_OH_columbianus_OR; FJ188868_OH_columbianus_OR; FJ188869_OH_columbianus_OR; FJ188870_OH_columbianus_OR; FJ188871_OH_columbianus_OR; FJ188872_OH_columbianus_OR; FJ188873_OH_columbianus_OR; FJ188874_OH_columbianus_OR; FJ188875_OH_columbianus_OR; FJ188876_OH_columbianus_OR; FJ188877_OH_sitkensis; FJ188878_OH_sitkensis; FJ188879_OH_sitkensis; FJ188880_OH_sitkensis; FJ188881_OH_eremicus; FJ188882_OH_eremicus; FJ188883_OH_sheldoni; FJ188884_OH_sheldoni; FJ188885_OH_crooki_TX; FJ188886_OH_crooki_TX; FJ188887_OH_crooki_TX; FJ188888_OH_crooki_TX; FJ188889_OH_hemionus_UT; FJ188890_OH_hemionus_UT; FJ188891_OH_hemionus_WA; FJ188892_OH_columbianus_WA; FJ188893_OH_columbianus_WA; FJ188894_OH_columbianus_WA; FJ188895_OH_columbianus_WA; FJ188896_OH_hemionus_WY; FJ188897_OH_hemionus_WY; FJ188898_OH_hemionus_WY; FJ188899_OH_hemionus_YK; FJ188900_OH_hemionus_YK; HM222707_OH; JN632670_OH; JN632671_OV; JN632672_OV; JN632673_OV; KM612271_OVver; KM612272_OVyuc; KM612273_OVtex; KM612274_OVsin; KM612275_; KM612276_OV; KM612277_OV; KM612278_OV; KM612279_OV; KT877248_OV_clavium; KT877249_OV_clavium; KT877250_OV_clavium; KT877251_OV_clavium; KT877252_OV_clavium; KT877253_OV_clavium; KT877254_OV_clavium; KT877255_OV_clavium; KT877256_OV_clavium; KT877257_OV_clavium; KT877258_OV_clavium; KT877259_OV_clavium; KT877260_OV_clavium; KT877261_OV_clavium; KT877262_OV_clavium; KT877263_OV_clavium; KT877264_OV_clavium; KT877265_OV_clavium; KT877266_OV_clavium; KT877267_OV_clavium; KT877268_OV_clavium; KT877269_OV_clavium; KT877270_OV_clavium; KT877271_OV_clavium; KT877272_OV_clavium; KT877273_OV_clavium; KT877274_OV_clavium; KT877275_OV_clavium; KT877276_OV_clavium; KT877277_OV_clavium; KT877278_OV_clavium; KT877279_OV_clavium; KT877280_OV_clavium; KT877281_OV_clavium; KT877282_OV; KT877283_OV; KT877284_OV; KT877285_OV; KT877286_OV; KT877287_OV; KT877288_OV; KT877289_OV; KT877290_OV; KT877291_OV; KT877292_OV; KT877293_OV; KT877294_OV; KT877295_OV; KT877296_OV; KT877297_OV; KT877298_OV; KT877299_OV; KT877300_OV; KT877301_OV; KT877302_OV; KT877303_OV; KT877304_OV; KT877305_OV; KT877306_OV; KT877307_OV; KT877308_OV; KT877309_OV; KT877310_OV; KT877311_OV; KT877312_OV; KT877313_OV; KT877314_OV; KT877315_OV; KT877316_OV; KT877317_OV; KT877318_OV; KT877319_OV5; KT877320_OV; KT877321_OV; KT877322_OV; KT877323_OV; KT877324_OV; KT877325_OV; KT877326_OV; KT877327_OV; KT877328_OV; KT877329_OV; KT877330_OV; KT877331_OV; KT877332_OV; KT877333_OV; KT877334_OV; KT877335_OV; KT877336_OV; KT877337_OV; KT877338_OV; KT877339_OV; KT877340_OV; KT877341_OV; KT877342_OV; KT877343_OV; KT877344_OV; NC_020729_OH; AJ000029_Rangifer; MN390611-390813 (samples from Nebraska, Minnesota and New York).

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Klicka, L.B., Najar, N., Vázquez-Miranda, H. et al. Relationships among North American deer based on mitochondrial DNA and ultraconserved elements, with comments on mito-nuclear discordance. Mamm Res 69, 245–255 (2024). https://doi.org/10.1007/s13364-024-00739-0

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