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Cranial geometric morphometrics of jumping mice (Genera: Eozapus, Napaeozapus, and Zapus; Zapodinae, Rodentia): Implications for subspecies conservation

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Abstract

Jumping mice (subfamily Zapodinae) occur across most of North America (Zapus and Napaeozapus) and in confined regions in China (Eozapus). Recent molecular phylogenies have revised their taxonomy, raising some subspecies to full species and synonymizing others. This taxonomic revision has implications for subspecies conservation and management, since Z. hudsonius preblei and Z. h. luteus are legally protected by the United States federal Endangered Species Act (ESA), while Z. h. campestris and Z. trinotatus orarius are conserved in parts of their range. Several molecular studies have either synonymized Z. h. preblei with Z. h. campestris (and Z. h. intermedius) or grouped it with Z. h. alascensis and Z. h. tenellus as a widely distributed “Northern” lineage, arguing against its continued legal protection. However, genetic differentiation is a proxy for historical but not always adaptive distinctiveness, and the ESA considers both for conservation (i.e., Evolutionarily Significant Units). This study uses geometric morphometrics to compare adaptive distinctiveness of jumping mice subspecies. This compares scaled cranial shape, leading to insights that differ from linear measurements. For broader insights, cranial morphology was compared within jumping mice and with the closely related birch mice. Subspecies pairs within the three traditionally accepted Zapus species were ranked in order morphometric distinctiveness. The most distinct pair was found to be Z. h. preblei vs. Z. h. alascensis, members of the same genetic lineage. Other morphometrically distinct subspecies pairs were parts of the same or different genetic lineages, some having been elevated to full species. Other members of especially distinct pairs include Z. princeps oregonus, Z. p. saltator, Z. p. cinereus, Z. p. minor, Z. p. pacificus, and Z. p. idahoensis. Other aspects of adaptive distinctiveness should be examined in these subspecies for validation and to prioritize conservation efforts.

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All data are in the online supplementary material.

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Notes

  1. Source: The International Union for Conservation of Nature Red List of Threatened Species. Information is based on the species level (no conservation information is available for the subspecies level).

  2. Source: The International Union for Conservation of Nature Red List of Threatened Species. Information is based on the species S. loriger which is sometimes considered to be the older synonym than S. nordmanni.

  3. Source: The U.S. Fish & Wildlife Service (Environmental Conservation Online System).

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Acknowledgements

This project would not have been possible without access to zoological specimens in the visited natural history museums. For this, I thank Ms. Marisa Surovy, Ms. Eleanor Hoeger, and Ms. Eileen Westwig from the AMNH; Dr. Bruce Patterson, Dr. Lawrence Heaney, Dr. Adam Ferguson, Mr. John Phelps, Mr. William Stanley, and Ms. Lauren Smith from the FMNH; Ms. Candace McCaffery and Dr. David Reed from UF; Dr. Christopher Conroy, Dr. James Patton, and Dr. Eileen Lacey from the MVZ; and Mr. Darrin Lunde and Dr. Michael Carleton from the USNM. I also thank the editor Dr. Joyce Prado and two anonymous reviewers for providing extremely detailed and helpful comments that I believe greatly improved the quality of the final version of the manuscript. Kuwait University funded some of the travel expenses as part of a scientific leave that took place between 2019 and 2020. No grant funding was received for this project.

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The sole author BHA wrote all parts of the paper.

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Correspondence to Bader H. Alhajeri.

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Appendix 1

Appendix 1

The specimens included in this study (n = 257) along with their scientific authors, sample sizes, and conservation status. See the Materials and methods for museum abbreviations.

Eozapus setchuanus setchuanus Pousargues, 1896 (n = 1) [Least ConcernFootnote 1].

AMNH 113580.

Eozapus setchuanus vicinus Thomas, 1912 (n = 3) [Least Concern1].

FMNH 36068; USNM 240762, 240900.

Napaeozapus insignis gaspensis Anderson, 1942 (n = 1) [Least Concern1].

FMNH 200135.

Napaeozapus insignis insignis Miller, 1891 (n = 35) [Least Concern1].

FMNH 200136, 200137, 200138, 200139, 200140, 200141, 200142, 200143, 200154, 200155, 200156, 200157, 200158, 200159, 200160, 200161, 200162, 200163, 200164, 200165, 200180, 200181, 200182, 200183, 200184, 200185, 200187, 200188, 200205, 200208, 200209; MVZ 101049, 96835, 96883, 96887.

Sicista betulina ssp. Pallas, 1779 (n = 4) [Least Concern1].

AMNH 178814, 206586; FMNH 92942; USNM 257391.

Sicista concolor flavus True, 1894 (n = 7) [Least Concern1].

FMNH 21913; USNM 173794, 173795, 173797, 173806, 173807, 173808.

Sicista concolor leathemi Thomas, 1893 (n = 16) [Least Concern1].

USNM 354390, 354393, 354394, 354395, 354396, 354397, 354398, 354399, 354400, 354401, 354402, 354403, 354404, 354405, 354406, 354407.

Sicista napaea ssp. Hollister, 1912 (n = 1) [Least Concern1].

AMNH 206587.

Sicista subtilis nordmanni Keyserling & Blasius, 1840 (n = 1) [VulnerableFootnote 2].

USNM 122119.

Sicista subtilis subtilis Pallas, 1773 (n = 1) [Least Concern1].

AMNH 206588.

Zapus hudsonius acadicus Dawson, 1856 (n = 27) [Least Concern1].

FMNH 200218, 200219, 200220, 200222, 200223, 200224, 200225, 200227, 200228, 200229, 200231, 200238, 200239, 200240, 200241, 80061; USNM 118027, 118030, 149038, 149041, 283458, 283461, 511145, 81106, 83746, 83748, 96933.

Zapus hudsonius alascensis Merriam, 1897 (n = 5) [Least Concern1].

USNM 119205, 119206, 119737, 119738, 73586.

Zapus hudsonius americanus Barton, 1799 (n = 17) [Least Concern1].

MVZ 167703, 96834, 96880, 96881; USNM 173175, 192512, 202781, 241015, 241016, 243269, 252763, 274029, 288295, 288296, 288332, 290495, 99458.

Zapus hudsonius campestris Preble, 1899 (n = 7) [Least Concern1].

FMNH 53767, 53768, 53770, 53771, 53772, 53773, 53774.

Zapus hudsonius preblei Krutzsch, 1954(n = 7) [EndangeredFootnote 3].

FMNH 11263, 11264, 11265, 11267, 11268, 11269, 11271.

Zapus princeps cinereus Hall, 1931 (n = 6) [Least Concern1].

USNM 170070, 170071, 170075, 170076, 170077, 170112.

Zapus princeps idahoensis Davis, 1934 (n = 10) [Least Concern1].

USNM 169209, 169212, 67298, 67519, 67520, 67521, 67522, 67523, 67524, 67526.

Zapus princeps minor Preble, 1899 (n = 7) [Least Concern1].

FMNH 7333, 7335, 7336, 7337, 7338, 9504, 9505.

Zapus princeps oregonus Preble, 1899 (n = 4) [Least Concern1].

MVZ 84023, 84024, 84026, 84028.

Zapus princeps pacificus Merriam, 1897 (n = 6) [Least Concern1].

AMNH 124327; USNM 94799, 94800, 95176, 95453, 95616.

Zapus princeps princeps Allen, 1893 (n = 9) [Least Concern1].

UF 12731, 12734, 12741; USNM 485755, 485756, 485757, 485758, 485759, 485760.

Zapus princeps saltator Allen, 1899 (n = 4) [Least Concern1].

FMNH 105513, 105517, 105519, 105520.

Zapus princeps utahensis Hall, 1934 (n = 15) [Least Concern1].

FMNH 145965, 145966, 145968, 177553, 177554, 177555, 177556, 177557, 177558, 177559, 177560, 93983, 93984, 93986, 93987.

Zapus trinotatus eureka Howell, 1920 (n = 8) [Least Concern1].

FMNH 9523, 9524, 9526, 9530; MVZ 99663, 99665, 99667, 99671.

Zapus trinotatus montanus Merriam, 1897 (n = 21) [Least Concern1].

USNM 204634, 204635, 204636, 204637, 204638, 204639, 204640, 204641, 204642, 204646, 204648, 79766, 79767, 79858, 79859, 79860, 79861, 79862, 79984, 80223, 80443.

Zapus trinotatus trinotatus Rhoads, 1894 (n = 34) [Least Concern1].

FMNH 105507, 105508, 206993, 206994, 206995, 206997, 206998, 206999, 207000, 207001, 207002, 207004, 6052, 6055, 6059, 6063, 7209, 7210, 8199, 9507, 9508, 9517, 9518; USNM 140499, 20003, 242024, 242025, 242032, 242033, 73131, 73852, 97644, 97645, 97646.

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Alhajeri, B.H. Cranial geometric morphometrics of jumping mice (Genera: Eozapus, Napaeozapus, and Zapus; Zapodinae, Rodentia): Implications for subspecies conservation. J Mammal Evol 30, 713–734 (2023). https://doi.org/10.1007/s10914-023-09666-4

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