{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T09:58:20Z","timestamp":1782467900543,"version":"3.54.5"},"reference-count":81,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2025,7,3]],"date-time":"2025-07-03T00:00:00Z","timestamp":1751500800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000011","name":"Howard Hughes Medical Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008510","name":"University of Maryland","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008510","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    The biochemical complexity and evolutionary diversity of snake venom composition reflects adaptation to the diversity of prey in their diets. However, the genetic mechanisms underlying the evolutionary diversity of venoms are not well understood. Here, we explored the potential extent of and genetic basis for venom protein variation in the widely-distributed Western Diamondback rattlesnake (\n                    <jats:italic>Crotalus atrox<\/jats:italic>\n                    ). As in many rattlesnake venoms, metalloproteinases (SVMPs) are the major component of\n                    <jats:italic>C. atrox<\/jats:italic>\n                    venom, with three proteins belonging to three distinct major structural SVMP classes, MDC4, MAD3a, and MPO1, constituting the most abundant SVMPs. We found that while most venom proteins, including MDC4 and MAD3a, vary little among individuals, the MPO1 protein is completely absent from some animals, most commonly those from the western part of the species\u2019 geographic range. This distribution correlates with the previous finding of two distinct lineages within\n                    <jats:italic>C. atrox<\/jats:italic>\n                    and indicates that different ecological factors have shaped venom composition across the species\u2019 range. We further show that the loss of MPO1 expression is not due to transcriptional down-regulation, but to independent inactivating mutations at the locus, including whole gene deletion. The recurrent inactivation of a major toxin gene within a\n                    <jats:italic>C. atrox<\/jats:italic>\n                    population may reflect relaxed selection on the maintenance of\n                    <jats:italic>MPO1<\/jats:italic>\n                    function, but we also raise the possibility that the loss of venom components may be favored if there is a cost to producing a less effective toxin in protein-rich venoms.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0319316","type":"journal-article","created":{"date-parts":[[2025,7,3]],"date-time":"2025-07-03T13:37:25Z","timestamp":1751549845000},"page":"e0319316","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Loss of a major venom toxin gene in a Western Diamondback rattlesnake population"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2425-6567","authenticated-orcid":true,"given":"Noah L.","family":"Dowell","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Cahill","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7839-5458","authenticated-orcid":true,"given":"Sean B.","family":"Carroll","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,7,3]]},"reference":[{"issue":"6839","key":"pone.0319316.ref001","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1038\/35081193","article-title":"Co-evolution and plant resistance to natural enemies","volume":"411","author":"MD Rausher","year":"2001","journal-title":"Nature"},{"issue":"21","key":"pone.0319316.ref002","doi-asserted-by":"crossref","first-page":"5315","DOI":"10.1111\/mec.13389","article-title":"Fifty years of co-evolution and beyond: Integrating co-evolution from molecules to species","volume":"24","author":"D Carmona","year":"2015","journal-title":"Mol Ecol"},{"issue":"12","key":"pone.0319316.ref003","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1038\/s41576-020-0269-1","article-title":"Host-parasite co-evolution and its genomic signature","volume":"21","author":"D Ebert","year":"2020","journal-title":"Nat Rev Genet"},{"issue":"4","key":"pone.0319316.ref004","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.tree.2012.10.020","article-title":"Complex cocktails: the evolutionary novelty of venoms","volume":"28","author":"NR Casewell","year":"2013","journal-title":"Trends Ecol Evol"},{"issue":"1","key":"pone.0319316.ref005","doi-asserted-by":"crossref","DOI":"10.1186\/s12864-016-2755-6","article-title":"Dietary breadth is positively correlated with venom complexity in cone snails","volume":"17","author":"MA Phuong","year":"2016","journal-title":"BMC Genomics"},{"issue":"1829","key":"pone.0319316.ref006","article-title":"Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey","volume":"283","author":"ML Holding","year":"2016","journal-title":"Proc R Soc B Biol Sci"},{"issue":"4","key":"pone.0319316.ref007","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1007\/s00442-017-3882-8","article-title":"Evaluating local adaptation of a complex phenotype: reciprocal tests of pigmy rattlesnake venoms on treefrog prey","volume":"184","author":"SA Smiley-Walters","year":"2017","journal-title":"Oecologia"},{"issue":"10","key":"pone.0319316.ref008","doi-asserted-by":"crossref","first-page":"1513","DOI":"10.1111\/jeb.13347","article-title":"Local prey community composition and genetic distance predict venom divergence among populations of the northern Pacific rattlesnake (Crotalus oreganus)","volume":"31","author":"ML Holding","year":"2018","journal-title":"J Evol Biol"},{"issue":"12","key":"pone.0319316.ref009","doi-asserted-by":"crossref","DOI":"10.3390\/toxins11120711","article-title":"Coevolution of snake venom toxic activities and diet: evidence that ecological generalism favours toxicological diversity","volume":"11","author":"EL Davies","year":"2019","journal-title":"Toxins"},{"issue":"8","key":"pone.0319316.ref010","article-title":"Prey Shifts Drive Venom Evolution in Cone Snails","volume":"41","author":"TL Koch","year":"2024","journal-title":"Molecular Biology and Evolution"},{"issue":"11","key":"pone.0319316.ref011","article-title":"Venom trade-off shapes interspecific interactions, physiology, and reproduction","volume":"10","author":"JM Surm","year":"2024","journal-title":"Sci Adv"},{"issue":"8","key":"pone.0319316.ref012","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1016\/j.toxicon.2010.02.028","article-title":"Evolutionary trends in venom composition in the western rattlesnakes (Crotalus viridis sensu lato): toxicity vs. tenderizers","volume":"55","author":"SP Mackessy","year":"2010","journal-title":"Toxicon"},{"issue":"11","key":"pone.0319316.ref013","doi-asserted-by":"crossref","first-page":"309","DOI":"10.3390\/toxins8110309","article-title":"Rapid radiations and the race to redundancy: an investigation of the evolution of Australian elapid snake venoms","volume":"8","author":"T Jackson","year":"2016","journal-title":"Toxins"},{"issue":"8","key":"pone.0319316.ref014","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1016\/j.tips.2020.05.006","article-title":"Causes and Consequences of Snake Venom Variation","volume":"41","author":"NR Casewell","year":"2020","journal-title":"Trends Pharmacol Sci"},{"issue":"20","key":"pone.0319316.ref015","doi-asserted-by":"crossref","first-page":"10911","DOI":"10.1073\/pnas.1920011117","article-title":"The origin and diversification of a novel protein family in venomous snakes","volume":"117","author":"MW Giorgianni","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"18","key":"pone.0319316.ref016","doi-asserted-by":"crossref","first-page":"2434","DOI":"10.1016\/j.cub.2016.07.038","article-title":"The Deep Origin and Recent Loss of Venom Toxin Genes in Rattlesnakes","volume":"26","author":"NL Dowell","year":"2016","journal-title":"Curr Biol"},{"issue":"7","key":"pone.0319316.ref017","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2018.02.031","article-title":"Extremely Divergent Haplotypes in Two Toxin Gene Complexes Encode Alternative Venom Types within Rattlesnake Species","volume":"28","author":"NL Dowell","year":"2018","journal-title":"Curr Biol"},{"issue":"3","key":"pone.0319316.ref018","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/1367-8280(94)90059-0","article-title":"Regional variation in the presence of canebrake toxin in Crotalus horridus venom","volume":"107","author":"JL Glenn","year":"1994","journal-title":"Comp Biochem Physiol Pharmacol Toxicol Endocrinol"},{"issue":"9","key":"pone.0319316.ref019","doi-asserted-by":"crossref","first-page":"1758","DOI":"10.1016\/j.jprot.2010.06.001","article-title":"Snake venomics and antivenomics of Crotalus durissus subspecies from Brazil: assessment of geographic variation and its implication on snakebite management","volume":"73","author":"J Boldrini-Fran\u00e7a","year":"2010","journal-title":"J Proteomics"},{"issue":"9","key":"pone.0319316.ref020","doi-asserted-by":"crossref","first-page":"2576","DOI":"10.1016\/j.jprot.2012.02.035","article-title":"Venom variability and envenoming severity outcomes of the Crotalus scutulatus scutulatus (Mojave rattlesnake) from Southern Arizona","volume":"75","author":"DJ Massey","year":"2012","journal-title":"J Proteomics"},{"key":"pone.0319316.ref021","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.jprot.2014.01.013","article-title":"Intraspecific venom variation in the medically significant Southern Pacific Rattlesnake (Crotalus oreganus helleri): biodiscovery, clinical and evolutionary implications","volume":"99","author":"K Sunagar","year":"2014","journal-title":"J Proteomics"},{"issue":"1898","key":"pone.0319316.ref022","article-title":"When one phenotype is not enough: Divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species","volume":"286","author":"G Zancolli","year":"2019","journal-title":"Proc R Soc B Biol Sci"},{"issue":"9","key":"pone.0319316.ref023","doi-asserted-by":"crossref","DOI":"10.1111\/jeb.13907","article-title":"Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey","volume":"34","author":"KE Robinson","year":"2021","journal-title":"J Evol Biol"},{"issue":"1","key":"pone.0319316.ref024","doi-asserted-by":"crossref","DOI":"10.1186\/s12915-023-01626-x","article-title":"Snakes on a plain: biotic and abiotic factors determine venom compositional variation in a wide-ranging generalist rattlesnake","volume":"21","author":"CF Smith","year":"2023","journal-title":"BMC Biol"},{"issue":"13","key":"pone.0319316.ref025","doi-asserted-by":"crossref","first-page":"3405","DOI":"10.1111\/mec.13240","article-title":"Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)","volume":"24","author":"MJ Margres","year":"2015","journal-title":"Mol Ecol"},{"key":"pone.0319316.ref026","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.toxicon.2016.05.005","article-title":"Functional characterizations of venom phenotypes in the eastern diamondback rattlesnake (Crotalus adamanteus) and evidence for expression-driven divergence in toxic activities among populations","volume":"119","author":"MJ Margres","year":"2016","journal-title":"Toxicon"},{"issue":"4","key":"pone.0319316.ref027","doi-asserted-by":"crossref","DOI":"10.3390\/toxins8040093","article-title":"Hemorrhage caused by snake venom metalloproteinases: A journey of discovery and understanding","volume":"8","author":"JM Guti\u00e9rrez","year":"2016","journal-title":"Toxins"},{"issue":"12","key":"pone.0319316.ref028","doi-asserted-by":"crossref","first-page":"3016","DOI":"10.1111\/j.1742-4658.2008.06466.x","article-title":"Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity","volume":"275","author":"JW Fox","year":"2008","journal-title":"FEBS J"},{"issue":"4","key":"pone.0319316.ref029","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0003731","article-title":"Tissue localization and extracellular matrix degradation by PI, PII and PIII snake venom metalloproteinases: clues on the mechanisms of venom-induced hemorrhage","volume":"9","author":"C Herrera","year":"2015","journal-title":"PLoS Negl Trop Dis"},{"issue":"51","key":"pone.0319316.ref030","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2214880119","article-title":"A novel broad spectrum venom metalloproteinase autoinhibitor in the rattlesnake Crotalus atrox evolved via a shift in paralog function","volume":"119","author":"FP Ukken","year":"2022","journal-title":"Proc Natl Acad Sci"},{"issue":"18","key":"pone.0319316.ref031","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"H Li","year":"2018","journal-title":"Bioinformatics"},{"issue":"5","key":"pone.0319316.ref032","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/nbt.3519","article-title":"Near-optimal probabilistic RNA-seq quantification","volume":"34","author":"NL Bray","year":"2016","journal-title":"Nat Biotechnol"},{"issue":"10","key":"pone.0319316.ref033","doi-asserted-by":"crossref","first-page":"4288","DOI":"10.1093\/nar\/gks042","article-title":"Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation","volume":"40","author":"DJ McCarthy","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"pone.0319316.ref034","volume-title":"R: A language and environment for statistical computing","author":"RR Core Team","year":"2016"},{"issue":"1","key":"pone.0319316.ref035","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1186\/s13059-015-0670-9","article-title":"Split-alignment of genomes finds orthologies more accurately","volume":"16","author":"MC Frith","year":"2015","journal-title":"Genome Biol"},{"issue":"2","key":"pone.0319316.ref036","doi-asserted-by":"crossref","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve years of SAMtools and BCFtools","volume":"10","author":"P Danecek","year":"2021","journal-title":"GigaScience"},{"issue":"18","key":"pone.0319316.ref037","doi-asserted-by":"crossref","first-page":"8447","DOI":"10.1073\/pnas.91.18.8447","article-title":"Structural interaction of natural and synthetic inhibitors with the venom metalloproteinase, atrolysin C (form d)","volume":"91","author":"D Zhang","year":"1994","journal-title":"Proc Natl Acad Sci"},{"issue":"13","key":"pone.0319316.ref038","doi-asserted-by":"crossref","first-page":"2416","DOI":"10.1016\/j.febslet.2007.04.057","article-title":"Crystal structures of catrocollastatin\/VAP2B reveal a dynamic, modular architecture of ADAM\/adamalysin\/reprolysin family proteins","volume":"581","author":"T Igarashi","year":"2007","journal-title":"FEBS Lett"},{"issue":"6","key":"pone.0319316.ref039","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/s41592-018-0001-7","article-title":"Accurate detection of complex structural variations using single-molecule sequencing","volume":"15","author":"FJ Sedlazeck","year":"2018","journal-title":"Nat Methods"},{"issue":"6","key":"pone.0319316.ref040","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/nmeth.2474","article-title":"Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data","volume":"10","author":"CS Chin","year":"2013","journal-title":"Nature Methods"},{"issue":"7","key":"pone.0319316.ref041","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1038\/nbt.2280","article-title":"Hybrid error correction and de novo assembly of single-molecule sequencing reads","volume":"30","author":"S Koren","year":"2012","journal-title":"Nat Biotechnol"},{"issue":"6","key":"pone.0319316.ref042","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1038\/nbt.3238","article-title":"Assembling large genomes with single-molecule sequencing and locality-sensitive hashing","volume":"33","author":"K Berlin","year":"2015","journal-title":"Nat Biotechnol"},{"issue":"5","key":"pone.0319316.ref043","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1038\/s41587-019-0072-8","article-title":"Assembly of long, error-prone reads using repeat graphs","volume":"37","author":"M Kolmogorov","year":"2019","journal-title":"Nat Biotechnol"},{"issue":"6","key":"pone.0319316.ref044","doi-asserted-by":"crossref","first-page":"3055","DOI":"10.1021\/pr900249q","article-title":"Exploring the venom proteome of the western diamondback rattlesnake, Crotalus atrox, via snake venomics and combinatorial peptide ligand library approaches","volume":"8","author":"JJ Calvete","year":"2009","journal-title":"J Proteome Res"},{"issue":"1","key":"pone.0319316.ref045","doi-asserted-by":"crossref","first-page":"439","DOI":"10.32614\/RJ-2018-009","article-title":"Simple feature for R: standardized support for spatial vector data","volume":"10","author":"E Pebesma","year":"2018","journal-title":"R J"},{"key":"pone.0319316.ref046","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-24277-4","volume-title":"ggplot2: Elegant Graphics for Data Analysis","author":"H Wickham","year":"2016"},{"key":"pone.0319316.ref047","author":"Commission for Environmental Cooperation, Statistics Canada, United States Census Bureau, Instituto Nacional de Estad\u00edstica y Geograf\u00eda","year":"2022"},{"key":"pone.0319316.ref048","volume-title":"The IUCN Red List of Threatened Species","author":"Nature Serve, IUCN IUCN (International Union for Conservation of Nature)","year":"2007"},{"key":"pone.0319316.ref049","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.toxicon.2019.03.027","article-title":"Venom composition of adult Western Diamondback Rattlesnakes (Crotalus atrox) maintained under controlled diet and environmental conditions shows only minor changes","volume":"164","author":"CJ Rex","year":"2019","journal-title":"Toxicon"},{"key":"pone.0319316.ref050","author":"National Atlas of the United States","year":"2002"},{"issue":"17","key":"pone.0319316.ref051","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2015579118","article-title":"Phylogenetically diverse diets favor more complex venoms in North American pitvipers","volume":"118","author":"ML Holding","year":"2021","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pone.0319316.ref052","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.ympev.2014.12.006","article-title":"Incipient speciation with biased gene flow between two lineages of the Western Diamondback Rattlesnake (Crotalus atrox)","volume":"83","author":"DR Schield","year":"2015","journal-title":"Mol Phylogenet Evol"},{"issue":"2","key":"pone.0319316.ref053","doi-asserted-by":"crossref","DOI":"10.3390\/toxins12020074","article-title":"Diet breadth mediates the prey specificity of venom potency in snakes","volume":"12","author":"K Lyons","year":"2020","journal-title":"Toxins"},{"issue":"4","key":"pone.0319316.ref054","doi-asserted-by":"crossref","DOI":"10.3390\/toxins15040251","article-title":"Diversity Begets Diversity When Diet Drives Snake Venom Evolution, but Evenness Rather Than Richness Is What Counts","volume":"15","author":"R Schaeffer","year":"2023","journal-title":"Toxins"},{"key":"pone.0319316.ref055","doi-asserted-by":"crossref","first-page":"503","DOI":"10.2307\/3669867","article-title":"Food habits of the western diamondback rattlesnake, Crotalus atrox, in Texas (Viperidae)","volume":"20","author":"RA Beavers","year":"1976","journal-title":"The Southwestern Naturalist"},{"key":"pone.0319316.ref056","first-page":"99","article-title":"Use of a mammalian resource by a Chihuahuan snake community","volume-title":"Woodcock ecology and management: papers from the seventh Woodcock Symposium held at the Pennsylvania State University, University Park, Pennsylvania, 28-30 October 1980","author":"RP Reynolds","year":"1981"},{"key":"pone.0319316.ref057","author":"CL Spencer","year":"2003"},{"issue":"4","key":"pone.0319316.ref058","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1894\/0038-4909-58.4.502","article-title":"Lagomorphs as prey of western diamond-backed rattlesnakes (Crotalus atrox) in Arizona","volume":"58","author":"CL Loughran","year":"2013","journal-title":"Southwest Nat"},{"key":"pone.0319316.ref059","doi-asserted-by":"crossref","first-page":"137","DOI":"10.2307\/3627861","article-title":"Food habits in Oklahoma Crotalus atrox in fall and early spring","volume":"94","author":"GR Pisani","year":"1991","journal-title":"Trans Kans Acad Sci"},{"issue":"6","key":"pone.0319316.ref060","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1016\/S0041-0101(98)00207-4","article-title":"The antihemorrhagic factor of the Mexican ground squirrel, (Spermophilus mexicanus)","volume":"37","author":"RR Martinez","year":"1999","journal-title":"Toxicon"},{"issue":"6","key":"pone.0319316.ref061","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/0041-0101(79)90234-4","article-title":"The resistance of three species of warm-blooded animals to Western diamondback rattlesnake (Crotalus atrox) venom","volume":"17","author":"JC Perez","year":"1979","journal-title":"Toxicon"},{"key":"pone.0319316.ref062","first-page":"1","article-title":"Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin genes","author":"NR Casewell","year":"2011","journal-title":"Mol Biol Evol"},{"issue":"9","key":"pone.0319316.ref063","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/s41559-022-01829-5","article-title":"The roles of balancing selection and recombination in the evolution of rattlesnake venom","volume":"6","author":"DR Schield","year":"2022","journal-title":"Nat Ecol Evol"},{"issue":"1","key":"pone.0319316.ref064","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-023-35794-9","article-title":"Micro and macroevolution of sea anemone venom phenotype","volume":"14","author":"EG Smith","year":"2023","journal-title":"Nat Commun"},{"issue":"9","key":"pone.0319316.ref065","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.tree.2009.03.010","article-title":"Relaxed selection in the wild","volume":"24","author":"DC Lahti","year":"2009","journal-title":"Trends Ecol Evol"},{"issue":"4","key":"pone.0319316.ref066","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1643\/0045-8511(2006)6[818:COPVIT]2.0.CO;2","article-title":"Cost of producing venom in three North American pitviper species","volume":"2006","author":"MD McCue","year":"2006","journal-title":"Copeia"},{"issue":"1","key":"pone.0319316.ref067","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1186\/s12915-020-00855-8","article-title":"Some like it hot: population-specific adaptations in venom production to abiotic stressors in a widely distributed cnidarian","volume":"18","author":"MY Sachkova","year":"2020","journal-title":"BMC Biol"},{"issue":"3","key":"pone.0319316.ref068","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1093\/icb\/28.3.863","article-title":"Energy Allocation in Mammalian Reproduction","volume":"28","author":"JL Gittleman","year":"1988","journal-title":"Am Zool"},{"key":"pone.0319316.ref069","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1242\/jeb.120402","article-title":"Size dependence in non-sperm ejaculate production is reflected in daily energy expenditure and resting metabolic rate","volume":"218","author":"CR Friesen","year":"2015","journal-title":"J Exp Biol"},{"issue":"1","key":"pone.0319316.ref070","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s00239-004-0138-0","article-title":"Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii)","volume":"60","author":"M Li","year":"2005","journal-title":"J Mol Evol"},{"issue":"4","key":"pone.0319316.ref071","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2014634118","article-title":"The tiger rattlesnake genome reveals a complex genotype underlying a simple venom phenotype","volume":"118","author":"MJ Margres","year":"2021","journal-title":"Proc Natl Acad Sci"},{"issue":"1","key":"pone.0319316.ref072","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1086\/302219","article-title":"When less is more: gene loss as an engine of evolutionary change","volume":"64","author":"MV Olson","year":"1999","journal-title":"Am J Hum Genet"},{"issue":"7","key":"pone.0319316.ref073","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1038\/nrg.2016.39","article-title":"Evolution by gene loss","volume":"17","author":"R Albalat","year":"2016","journal-title":"Nat Rev Genet"},{"issue":"3","key":"pone.0319316.ref074","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/s41437-021-00403-2","article-title":"The population genomics of adaptive loss of function","volume":"126","author":"JG Monroe","year":"2021","journal-title":"Heredity (Edinb)"},{"issue":"2","key":"pone.0319316.ref075","doi-asserted-by":"crossref","DOI":"10.1093\/molbev\/msaf012","article-title":"Population Genomics of Premature Termination Codons in Cavefish With Substantial Trait Loss","volume":"42","author":"EY Roback","year":"2025","journal-title":"Mol Biol Evol"},{"issue":"8","key":"pone.0319316.ref076","doi-asserted-by":"crossref","first-page":"3036","DOI":"10.1073\/pnas.1818504116","article-title":"Convergent gene losses illuminate metabolic and physiological changes in herbivores and carnivores","volume":"116","author":"N Hecker","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"9","key":"pone.0319316.ref077","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.aaw6671","article-title":"Genes lost during the transition from land to water in cetaceans highlight genomic changes associated with aquatic adaptations","volume":"5","author":"M Huelsmann","year":"2019","journal-title":"Sci Adv"},{"issue":"1","key":"pone.0319316.ref078","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-018-03667-1","article-title":"A genomics approach reveals insights into the importance of gene losses for mammalian adaptations","volume":"9","author":"V Sharma","year":"2018","journal-title":"Nature Communications"},{"issue":"26","key":"pone.0319316.ref079","doi-asserted-by":"crossref","first-page":"12919","DOI":"10.1073\/pnas.1903925116","article-title":"Evolution of sex ratio through gene loss","volume":"116","author":"D Yin","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"12","key":"pone.0319316.ref080","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.abm6494","article-title":"Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding","volume":"8","author":"M Blumer","year":"2022","journal-title":"Sci Adv"},{"issue":"1","key":"pone.0319316.ref081","doi-asserted-by":"crossref","DOI":"10.1186\/s12915-022-01243-0","article-title":"Gene losses may contribute to subterranean adaptations in naked mole-rat and blind mole-rat","volume":"20","author":"Z Zheng","year":"2022","journal-title":"BMC Biol"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0319316","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,3]],"date-time":"2025-07-03T13:37:42Z","timestamp":1751549862000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0319316"}},"subtitle":[],"editor":[{"given":"Karen","family":"de Morais-Zani","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,7,3]]},"references-count":81,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2025,7,3]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0319316","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.02.02.636150","asserted-by":"object"}]},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,3]]}}}