** mentored undergraduate † joint lead author
2026
[52] Neilsen D, Holding ML, Del Carlo RE, Everson KM, Ochsenrider K, Simison WB, Henderson J, Dearing MD, Hayes JP, Frese SA, Richards LA, Ferguson BS, Forbey JS, Matocq MD. 2026. Diet change reveals asymmetric response in gene expression and microbial composition across the digestive tract of two closely related herbivores. BMC Biology. https://doi.org/10.1186/s12915-026-02658-9
[51] Farleigh K, Highland DK, Alderman MG, Francioli Y, Hirst SR, Faber EM, Perry BW, Holding ML, Castañeda-Gaytan G, Borja M, Franz-Chávez H, Parkinson CL, Strickland JL, Margres MJ, Mackessy SP, Meik JM, Castoe TA, Schield DR. 2026. Evolution of genome-wide barriers to gene flow during complex speciation in rattlesnakes. Proceedings of the National Academy of Sciences of the United States of America 123: e2609058123. https://doi.org/10.1073/pnas.2609058123
[50] Holding ML, Pontius MHH, **Ward MS, Akhtar J, Crowell HL, Svilar D, Keeler KM, Haynes LM, Ginsburg D, Shavit JA. 2026. Deconstructing cardiovascular and coagulation- related traits links dietary ecology to multi-functional snake venom specificity. Evolution 80: 1035-1046, qpag036. https://doi.org/10.1093/evolut/qpag036
2025
[49] ** †Ward MS, †Holding ML, Haynes LM, Margres MJ, Matocq MD, Ginsburg D. 2025. Tandem duplication of serpin genes yields functional variation and snake venom inhibitors. Molecular Biology and Evolution 42: msaf290. https://doi.org/10.1093/molbev/msaf290
[48] Haynes LM, Holding ML, Woodard J, Siemieniak D, Ginsburg D. 2025. Thermodynamics and selection of the plasminogen activator inhibitor-1 latency transition. Journal of Biological Chemistry 301:110896. https://doi.org/10.1016/j.jbc.2025.110896
[47] †Holding ML, †Disharoon D, †Haynes LM, Chakravarthy Paruchuri B, Pontius MHH, Golden K, Shavit JA, Desch KC, Ginsburg D, Sen Gupta A, Cruz Y, †Drabeck DH. 2025. Comparative microfluidic and enzymatic analyses reveal multifaceted snake venom resistance and novel VWF behavior in the opossum Monodelphis domestica. PLoS One 20: e0332686. https://doi.org/10.1371/journal.pone.0332686
[46] Hogan MP, Holding ML, Nystrom GS, Lawrence KC, Broussard EM, Ellsworth SA, Mason AJ, Margres MJ, Gibbs HL, Parkinson CL, Rokyta DR. 2025. Life history and chromosome organization determine chemoreceptor gene expression in rattlesnakes. Journal of Heredity. 116: 617-631. https://doi.org/10.1093/jhered/esae078
[45] Holding ML, Kolora SRR, Smith JE, McDevitt SL, Sudmant PH, Tarvin RD. 2025. A genome assembly for a textbook mammalian study species, the California ground squirrel (Otospermophilus beecheyi). Journal of Heredity 2025: esaf045. https://doi.org/10.1093/jhered/esaf045
[44] Holding ML, Coconis A, Connors PK, Matocq MD, Dearing MD. 2025. Ambient temperature and toxic diets constrain snake venom resistance in a desert rodent. Biology Letters 21: 20250068
[43] Haynes LM, Holding ML, **DiGiovanni HL, Siemieniak D, Ginsburg D. 2025. High-throughput amino acid-level characterization of the interactions of plasminogen activator inhibitor-1 with variably divergent proteases. Protein Science 34: e70088. https://doi.org/10.1002/pro.70088
[42] Heptinstall TC, Rosales García RA, Rautsaw RM, Myers EA, Holding ML, Mason AJ, Hofmann EP, Schramer TD, Hogan MP, Borja M, Castañeda-Gaytán G, Feldman CR, Rokyta DR, Parkinson CL. 2025. Dietary breadth predicts toxin expression complexity in the venoms of North American gartersnakes. Integrative Organismal Biology 7: obaf003. https://doi.org/10.1093/iob/obaf003
[41] **Beimfohr C, Rivas Moreno L, **Anderson R, **Cardwell R, Seeman Z, Spry R, Holding M, Owens A, Denton R. 2025. Characterizing population structure and documenting rapid loss of genetic diversity in Chiricahua Leopard Frogs (Lithobates chiricahuensis) with high throughput microsatellite genotyping. Conservation Genetics 26: 293-306. https://doi.org/10.1007/s10592-024-01667-x
2024
[40] Hogan, MP, Holding, ML, Nystrom, GS, Colston, TJ, Bartlett, DA, Mason, AJ, Ellsworth, SA, Rautsaw, RM, Lawrence, KC, Strickland, JL, He, B, Fraser, P, Margres, MJ, Gilbert, DM, Gibbs, HL, Parkinson, CL, Rokyta, DR. 2024. The genetic regulatory architecture and epigenomic basis for age-related changes in rattlesnake venom. Proceedings of the National Academy of Science of the USA 121: e2313440121. https://doi.org/10.1073/pnas.2313440121
[39] Myers, EA, Rautsaw, RM, Borja, M, Jones, J, Grünwald, CI, Holding, ML, Grazziotin, F, Parkinson, CL. 2024. Phylogenomic discordance is driven by wide-spread introgression and incomplete lineage sorting during rapid species diversification within rattlesnakes (Viperidae: Crotalus and Sistrurus). Systematic Biology 73: 722- 741. https://doi.org/10.1093/sysbio/syae018
[38] Ellsworth SA, Rautsaw RM, Ward MJ, Holding ML, Rokyta DR. 2024. Selection across the three-dimensional structure of venom proteins from North American Scolopendromorph centipedes. Journal of Molecular Evolution 92: 505-524. https://doi.org/10.1007/s00239-024-10191-y
2023
[37] Brovkina, MV, Chapman, MA, Holding ML, Clowney, EJ. 2023. Emergence and influence of sequence bias in evolutionarily malleable, mammalian tandem arrays. BMC Biology 21: 179. https://doi.org/10.1186/s12915-023-01673-4
[36] Westeen, EP, Escalona, M, Holding, ML, Beraut, E, Fairbairn, C, Marimuthu, MPA Nguyen, O, Perri, R, Fisher, RN, Toffelmier, E Shaffer, HB, Wang, IJ. 2023. A genome assembly for the southern Pacific rattlesnake, Crotalus oreganus helleri, in the western rattlesnake species complex. Journal of Heredity 2023: esad045. https://doi.org/10.1093/jhered/esad045
[35] Rosales-García, RA, Rautsaw, RM, Hofmann EP, Grünwald, C, Franz-Chavez, H, Ahumada- Carrillo, IT, Ramirez-Chaparro, R, Angel del Torre-Loranca, M, Strickland, JL, Mason, AJ, Holding ML, Borja, M, Castañeda-Gaytan, G, Myers, EA, Sasa, M, Rokyta, DR, Parkinson, CL. 2023. Sequence divergence in venom genes within and between montane pitviper (Viperidae: Crotalinae: Cerrophidion) species is driven by mutation-drift equilibrium. Journal of Molecular Evolution 91: 514-535. https://doi.org/10.1007/s00239-023-10115-2
2022
[34] Holding ML, Trevine, VC, Zinenko, O, Strickland, JL, Rautsaw, RM, Mason, AJ, Hogan, MP, Parkinson, CL, Grazziotin, FG, Santana, SE, Davis, ME, Rokyta, DR. 2022. Evolutionary allometry and ecological correlates of fang length evolution in vipers. Proceedings of the Royal Society B 289:20221132. https://doi.org/10.1098/rspb.2022.1132
[33] Mason, AJ, Holding, ML, Rautsaw, RM, Rokyta, DR, Parkinson, CL, Gibbs, HL. 2022. Venom gene sequence diversity and expression jointly shape diet adaptation in pitvipers. Molecular Biology and Evolution 39: msac082. https://doi.org/10.1093/molbev/msac082
[32] Schield, D.R., B.W. Perry, R.H. Adams, Holding, ML, Z.L. Nikolakis, S.S. Gopalan, C.F. Smith, J.M. Parker, J.M. Meik, S.P. Mackessy, and T.A. Castoe. 2022. The roles of balancing selection and recombination in the evolution of rattlesnake venom. Nature Ecology & Evolution 6: 1367–1380. https://doi.org/10.1038/s41559-022-01829-5
[31] Greenhalgh, R., Holding, ML, Orr, TJ, Henderson, JB, Parchman, TL, Matocq, MD, Dearing, MD. 2022 Trio-binned genomes of the woodrats Neotoma bryanti and N. lepida reveal novel gene islands and rapid copy number evolution of xenobiotic metabolizing cytochrome p450 genes. Molecular Ecology Resources 22, 2713– 2731. https://doi.org/10.1111/1755-0998.13650Digital Object Identifier (DOI)
[30] Ochoa, A, Hassinger, ATB, Holding, ML, and Gibbs HL. 2022. Genetic characterization of potential venom resistance proteins in California ground squirrels (Otospermophilus beecheyi) using transcriptome analyses. J. Experimental Zoology B: Molecular and Developmental Evolution. 10.1002/jez.b.23145. https://doi.org/10.1002/jez.b.23145
2021
[29] Huttinger ZM, Haynes LM, Yee A, Kretz CA, Holding ML, Siemieniak DR, Lawrence DA, Ginsburg, D. 2021. Deep mutational scanning of the plasminogen activator inhibitor-1 functional landscape. Scientific Reports 11:18827. https://doi.org/10.1038/s41598-021-97871-7
[28] Holding ML, Strickland, JL, Rautsaw, RM, Mason, AJ, Hofmann, EP, Hogan, MP, Ellsworth, S, Nystrom, G, Margres, MM, Colston, TJ, Borja, M., Grünwald, C., Jones, J., Castañeda, G. Frietas-de-Sousa, .L, Moura-da-Silva, A, Azevedo, I, Grazziotin, FG, Gibbs, HL, Rokyta, DR, Parkinson, CL. 2021. Phylogenetically diverse diets favor more complex venoms in North American pitvipers. Proceedings of the National Academy of Science of the USA 118, e2015579118. https://doi.org/10.1073/pnas.2015579118
[27] Byer, NB, Holding, ML, Crowell, M., Pierson, TW, Dilts, TE, Shoemaker, KT, Matocq, MD. 2021. Adaptive divergence despite low effective population size in a peripherally isolated population of the pygmy rabbit (Brachylagus idahoensis. Molecular Ecology 30:4173–4188. https://doi.org/10.1111/mec.16040
[26] Robinson, KR, Holding, ML, Saviola, A, Whitford, MA, Clark, RC. 2021. Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey. Journal of Evolutionary Biology 34:1447–1465. https://doi.org/10.1111/jeb.13907
[25] Claunch, NC, Holding, ML, Frazier, JA, **Huff, EM, **Schonour, RB, Vernasco, B, Moore, IT, Rokyta, DR, Taylor, EN 2021. Experimental manipulation of corticosterone does not affect venom composition or functional activity in free- ranging rattlesnakes. Physiological and Biochemical Zoology. https://doi.org/10.1086/714936
2020
[24] **†Schonour, RB, **†Huff, EM, Holding, ML, Claunch, NM, Ellsworth, SA, Hogan, MP, Wray, K, McGivern, J, Margres, MJ, Colston, TJ, Rokyta, DR. 2020. Gradual and discrete ontogenetic shifts in rattlesnake venom composition and assessment of hormonal and ecological correlates. Toxins 12: 659. https://doi.org/10.3390/toxins12100659
[23] Holding, ML, Sovic, MG, Colston, TC, Gibbs, HL. 2020. The scales of coevolution: comparative phylogeography and genetic demography of a locally adapted venomous predator and its prey. Biological Journal of the Linnean Society 132, 297-317. https://doi.org/10.1093/biolinnean/blaa192
[22] †Holding, ML, †Putman, BJ, **Kong, LM, Smith, JE, Clark, RW. 2020. Physiological stress integrates resistance to rattlesnake venom and the onset of risky foraging in California ground squirrels. Toxins 12: 617. https://doi.org/10.3390/toxins12100617
[21] Gibbs, HL, Sanz, L, Pérez, A, Ochoa, A, Hassinger, ATB, Holding, ML, Calvete, JJ. 2020. The molecular basis of venom resistance in a rattlesnake‐squirrel predator‐prey system. Molecular Ecology 29: 2871-2888. https://doi.org/10.1111/mec.15529
[20] Freitas-de-Sousa, LA, Nachtigall, P, Portes-Jenior, JA, Holding, ML, Nystrom, GS, Ellsworth, SA, Guimarãs, NC, Tioyama, E, Ortiz, F, Silva BR, Kunz, TS, Junqueira-de-Azevedo, ILM, Grazzitin, FG, Rokyta, DR, Moura-da-Silva, AM. 2020. Size matters: an evaluation of the molecular basis of ontogenetic modifications in the composition of Bothrops jararacussu snake venom. Toxins 12: 791. https://doi.org/10.3390/toxins12120791
[19] Rautsaw, RM, Hofmann, EP, Margres, MM, Holding, ML, Strickland, JL, Mason, AJ, Rokyta, DR, Parkinson, CL. 2019. Intraspecific sequence and gene expression variation contribute little to venom diversity in Sidewinder Rattlesnakes. Proceedings of the Royal Society B: Biological Sciences 286: 20190810. https://doi.org/10.1098/rspb.2019.0810
[18] Goetz SM, Piccolomini S, Hoffman M, Bogan J, Holding ML, Mendonca MT, Steen DA. 2019. Serum-based inhibition of pitviper venom by Eastern Indigo Snakes (Drymarchon couperi). Biology Open. https://doi.org/10.1242/bio.040964
2018
[17] Holding ML, Margres MM, Mason AJ, Parkinson CL, Rokyta DR. 2018. Evaluating the performance of de novo assembly methods for venom-gland transcriptomes. Toxins 10: 10060249. https://doi.org/10.3390/toxins10060249
[16] Hofmann EP, Rautsaw RM, Stickland JL, Holding ML, Hogan MP, Mason AJ, Rokyta DR, Parkinson CL .2018. Comparative venom-gland transcriptomics and venom proteomics of four Sidewinder Rattlesnake (Crotalus cerastes) lineages reveal little differential expression despite individual variation. Scientific Reports 8: 15534. https://doi.org/10.1038/s41598-018-33943-5
[15] Holding ML, Margres MM, Rokyta DR, Gibbs HL. 2018. Local prey community composition and genetic distance predict venom divergence among populations of the northern Pacific rattlesnake (Crotalus oreganus). Journal of Evolutionary Biology 31: 1513–1528. https://doi.org/10.1111/jeb.13347
[14] McCluskey EM, Matthew SN, Ligocki IY, Holding ML, Lipps GL Jr, Hetherington TE. 2018. The importance of historical land use in the maintenance of early successional habitat for a threatened rattlesnake. Global Ecology and Conservation 13, e00370. doi.org/10.1016/j.gecco.2017.e00370.
2017
[13] Claunch NC, Holding ML, Escallon C, Vernasco B, Moore IT, Taylor EN. 2017. Good vibrations: Assessing the stability of snake venom composition after researcher-induced disturbance in the laboratory. Toxicon 133: 127-135. https://doi.org/10.1016/j.toxicon.2017.05.010
[12] **Hudson P, Denton RD, Holding ML, Gibbs HL. 2017. Repeatability of locomotor endurance in the Smallmouth Salamander (Ambystoma texanum). Herpetological Review 47: 583-586.
2016
[11] †Holding ML, †Drabeck DH , Jansa SA, and Gibbs HL. 2016. Venom resistance as a model for understanding the molecular basis of coevolutionary adaptations. Invited review for Integrative and Comparative Biology 56: 1032-1043. https://doi.org/10.1093/icb/icw082
[10] Holding ML, Biardi JE, Gibbs HL. 2016. Coevolution of venom function and prey resistance in a rattlesnake predator and its squirrel prey. Proceedings of the Royal Society B: Biological Sciences 283:28-41. https://doi.org/10.1098/rspb.2015.2841
[9] **Saccucci M, Denton RD, Holding ML, Gibbs HL. 2016. Polyploid unisexual salamanders have higher tissue regeneration rates than diploid sexual relatives. Journal of Zoology 300: 77-81. https://doi.org/10.1111/jzo.12339
[8] †**Pomento AM, †**Perry BW, Denton RD, Gibbs HL, Holding ML. 2016. No safety in the trees: Local and species-level adaptation of an arboreal squirrel to the venom of sympatric rattlesnakes. Toxicon 118:149-155. https://doi.org/10.1016/j.toxicon.2016.05.003
[7] Holding ML, **Kern EH, Denton RD, Gibbs HL. 2016. Fixed prey cue preferences among Dusky Pigmy Rattlesnakes (Sistrurus miliarius barbouri) raised on different long-term diets. Evolutionary Ecology 30:1-7. https://doi.org/10.1007/s10682-015-9787-2
2014
[6] †Holding ML,†Denton RD , Kulesza A, Ridgway JS. 2014. Confronting scientific misconceptions by fostering a classroom of scientists in the introductory biology lab. The American Biology Teacher 76: 218-523. https://doi.org/10.1525/abt.2014.76.8.5
[5] Holding ML, Owen DAS, Taylor EN. 2014. Evaluating the thermal effects of translocation in a large-bodied pitviper. Journal of Experimental Zoology A 321, 442-449. https://doi.org/10.1002/jez.1876
[4] Owen DAS, Carter E, Holding ML, Islam K, Moore IT. 2014. Roads are associated with a blunted stress response in a North American pit viper. General and Comparative Endocrinology 202:87-92. https://doi.org/10.1016/j.ygcen.2014.04.020
[3] Holding ML, Frazier JA, Pollock N, **Dorr SW, et al. 2014. Wet- and dry-season steroid hormone profiles and stress reactivity of an insular dwarf snake, the Hog Island Boa (Boa constrictor imperator). Physiological and Biochemical Zoology 87:363-373. https://doi.org/10.1086/675938
[2] Holding ML, Frazier JA, **Dorr SW, Henningsen SN, Moore IT, and Taylor EN. 2014. The physiological and behavioral effects of repeated handling and short-distance translocation on free-ranging Northern Pacific rattlesnakes (Crotalus o. oreganus). Journal of Herpetology48: 233-239. http://www.jstor.org/stable/43287438
2012
[1] Holding ML, Frazier JA, Taylor EN, Strand CR .2012. Experimentally-altered navigational demands induce changes in the cortical forebrain of free-ranging Northern Pacific Rattlesnakes (Crotalus o. oreganus). Brain, Behavior, and Evolution 79:144-154. https://doi.org/10.1159/000335034