Abstract
The sequestration by neotropical poison frogs (Dendrobatidae) of an amazing array of defensive alkaloids from oribatid soil mites has motivated an exciting research theme in chemical ecology, but the details of mite-to-frog transfer remain hidden. To address this, McGugan et al. (2016, Journal of Chemical Ecology 42:537–551) used the little devil poison frog (Oophaga sylvatica) and attempted to simultaneously characterize the prey mite alkaloids, the predator skin alkaloids, and identify the mites using DNA sequences. Heethoff et al. (2016, Journal of Chemical Ecology 42:841–844) argued that none of the mite families to which McGugan et al. allocated the prey was thought to possess alkaloids. Heethoff et al. concluded from analyses including additional sequences that the mite species were unlikely to be close relatives of the defended mites. We re-examine this by applying more appropriate phylogenetic methods to broader and denser taxonomic samples of mite sequences using the same gene (CO1). We found, over trees based on CO1 datasets, only weak support (except in one case) for branches critical to connecting the evolution of alkaloid sequestration with the phylogeny of mites. In contrast, a well-supported analysis of the 18S ribosomal gene suggests at least two independent evolutionary origins of oribatid alkaloids. We point out impediments in the promising research agenda, namely a paucity of genetic, chemical, and taxonomic information, and suggest how phylogenetics can elucidate at a broader level the evolution of chemical defense in prey arthropods, sequestration by predators, and the impact of alkaloids on higher-order trophic interactions.
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References
Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45. https://doi.org/10.1111/j.1469-8137.2011.04049.x
Alberti G, Norton R, Addis J, Fernandez N, Franklin E, Kratzmann M, Moreno A, Ribeiro E, Weigmann G, Woas S (1997) Porose areas and related organs in oribatid mites (Oribatida). In: Mitchell R, Horn DJ, Needham GR, Welbourn WC (eds) Acarology IX. Proceedings of the 9th international congress of acarology. Ohio Biological Survey, Columbus, Ohio, pp 277–283
Alvardo JB, Alvarez A, Saporito RA (2013) Oophaga pumilio predation by Baryphthengus martii. Herpetol Rev 44:298
AmphibiaWeb (2021) Information on amphibian biology and conservation. Berkeley, California. https://www.amphibiaweb.org. Accessed 12 November 2021
Aoki J, Takaku G, Ito F (1994) Aribatidae, a new myrmecophilous oribatid mite family from Java. Int J Acarology 20:3–10. https://doi.org/10.1080/01647959408683994
Arabi J, Judson MLI, Deharveng L, Lourenço WR, Cruaud C, Hassanin A (2012) Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): Detecting new mitogenomic rearrangements. J Mol Evol 74:81–95. https://doi.org/10.1007/s00239-012-9490-7
Arribas P, Andújar C, Moraza ML, Linard B, Emerson BC, Vogler AP (2020) Mitochondrial metagenomics reveals the ancient origin and phylodiversity of soil mites and provides a phylogeny of the Acari. Mol Biol Evol 37:683–694. https://doi.org/10.1093/molbev/msz255
Berenbaum MR (1995) The chemistry of defense: theory and practice. Proc Natl Acad Sci U S A 92:2–8. https://doi.org/10.1073/pnas.92.1.2
Bik HM (2017) Let’s rise up to unite taxonomy and technology. PLoS Biol 15(8):e2002231. https://doi.org/10.1371/journal.pbio.2002231
Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crust Biol 29:96–110. https://doi.org/10.1651/08-3020.1
Chernomor O, von Haeseler A, Minh BQ (2016) Terrace-aware data structure for phylogenomic inference from supermatrices. Syst Biol 65:997–1008. https://doi.org/10.1093/sysbio/syw037
Daly JW, Garraffo HM, Spande TF, Jaramillo C, Rand AS (1994) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol 20:943–955. https://doi.org/10.1007/BF02059589
Darst CR, Menéndez-Guerrero PA, Coloma LA, Cannatella DC (2005) Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. Am Nat 165:56–69. https://doi.org/10.1086/426599
Davic RD, Welsh HH (2004) On the ecological role of salamanders. Annu Rev Ecol Evol Syst 12:405–434. https://doi.org/10.1146/annurev.ecolsys.35.112202.130116
Drew LW (2011) Are we losing the science of taxonomy? As need grows, numbers and training are failing to keep up. Bioscience 61:942–946. https://doi.org/10.1525/bio.2011.61.12.4
Dumbacher JP (1999) Evolution of toxicity in pitohuis: I. Effects of homobatrachotoxin on chewing lice (order Phthiraptera). Auk 116:957–963. https://doi.org/10.2307/4089675
Dumbacher JP (2014) A taxonomic revision of the genus Pitohui Lesson, 1831 (Oriolidae), with historical notes on names. Bull Bri Ornithol Club 134:19–22
Dumbacher JP, Fleischer RC (2001) Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds. Proc Biol Sci 268:1971–1976. https://doi.org/10.1098/rspb.2001.1717
Dumbacher JP, Beehler BM, Spande TF, Garraffo HM, Daly JW (1992) Homobatrachotoxin in the genus Pitohui: chemical defense in birds? Science 258:799–801. https://doi.org/10.1126/science.1439786
Dumbacher JP, Wako A, Derrickson SR, Samuelson A, Spande TF, Daly JW (2004) Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds. Proc Natl Acad Sci U S A 101:15857–15860. https://doi.org/10.1073/pnas.0407197101
Dumbacher JP, Deiner K, Thompson L, Fleischer RC (2008) Phylogeny of the avian genus Pitohui and the evolution of toxicity in birds. Mol Phylogenet Evol 49:774–781. https://doi.org/10.1016/j.ympev.2008.09.018
Feldman CR, Brodie ED Jr, Brodie ED III, Pfrender ME (2009) The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc Natl Acad Sci U S A 106:13415–13420. https://doi.org/10.1073/pnas.0901224106
Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Biol 27:401–410. https://doi.org/10.1093/sysbio/27.4.401
Ferrer RP, Zimmer RK (2013) Molecules of keystone significance: crucial agents in ecology and resource management. Bioscience 63:428–438. https://doi.org/10.1525/bio.2013.63.6.5
Fritz G, Rand AS, DePamphilis CW (1981) The aposematically colored frog, Dendrobates pumilio, is distasteful to the large, predatory ant, Paraponera clavata. Biotropica 13:158–159. https://doi.org/10.2307/2387719
Geneious Prime (2021) Geneious Prime 2021.0.3 (https://www.geneious.com)
Groen SC, Whiteman NK (2021) Convergent evolution of cardiac-glycoside resistance in predators and parasites of milkweed herbivores. Curr Biol 31:R1465–R1466. https://doi.org/10.1016/j.cub.2021.10.025
Hebert PD, Cywinska A, Ball SL (2003) Biological identifications through DNA barcodes. Proc R Soc B 270:313–321. https://doi.org/10.1098/rspb.2002.2218
Hebert PD, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2:e312. https://doi.org/10.1371/journal.pbio.0020312
Heethoff M (2012) Regeneration of complex oil-gland secretions and its importance for chemical defense in an oribatid mite. J Chem Ecol 38:1116–1123. https://doi.org/10.1007/s10886-012-0169-8
Heethoff M, Norton RA, Raspotnig G (2016) Once again: oribatid mites and skin alkaloids in poison frogs. J Chem Ecol 42:841–844. https://doi.org/10.1007/s10886-016-0758-z
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh KS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281
Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Syst Biol 42:247–264. https://doi.org/10.1093/sysbio/42.3.247
Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52:131–138. https://doi.org/10.1080/10635150390192780
Huelsenbeck JP, Larget B, Alfaro M (2004) Bayesian phylogenetic model selection using reversible jump markov chain Monte Carlo. Mol Biol Evol 21:1123–1133. https://doi.org/10.1093/molbev/msh123
Ito F, Takaku G (1994) Obligate myrmecophily in an oribatid mite. Naturwissenschaften 81:180–182. https://doi.org/10.1007/BF01134538
Jones TH, Gorman JST, Snelling RR, Delabie JHQ, Blum MS, Garraffo HM, Jain P, Daly JW, Spande TF (1999) Further alkaloids common to ants and frogs: decahydroquinolines and a quinolizidine. J Chem Ecol 25:1179–1193. https://doi.org/10.1023/A:1020898229304
Jones M, Mandelik Y, Dayan T (2001) Coexistence of temporally partitioned spiny mice: roles of habitat structure and foraging behavior. Ecology 82:2164–2176. https://doi.org/10.2307/2680223
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Klimov PB, O’Connor BM, Chetverikov PE, Bolton SJ, Pepato AR, Mortazavi AL, Tolstikov AV, Bauchan GR, Ochoa R (2018) Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea), a long branch. Mol Phylogenet Evol 119:105–117. https://doi.org/10.1016/j.ympev.2017.10.017
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kurzava LM, Morin PJ (1998) Tests of functional equivalence: complementary roles of salamanders and fish in community organization. Ecology 79:477–489. https://doi.org/10.1890/0012-9658
Kuwahara Y (2004) Chemical ecology in astigmatid mites. In: Cardé R, Millar JG (eds) Advances in chemical ecology. Cambridge University Press, Cambridge, pp 76–109
Maddison WP, Maddison DR (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61 http://www.mesquiteproject.org
Marti CD, Steenhof K, Kochert MN, Marks JS (1993) Community trophic structure: the roles of diet, body size, and activity time in vertebrate predators. Oikos 67:6–18. https://doi.org/10.2307/3545090
Masuko K (1994) Specialized predation on oribatid mites by two species of the ant genus Myrmecina (Hymenoptera: Formicidae). Psyche 101:159–173. https://doi.org/10.1155/1994/96412
McGugan JR, Byrd GD, Roland AB, Caty SN, Kabir N, Tapia EE, Trauger SA, Coloma LA, O’Connell LA (2016a) Ant and mite diversity drives toxin variation in the little devil poison frog. J Chem Ecol 42:537–551. https://doi.org/10.1007/s10886-016-0715-x
McGugan JR, Byrd GD, Roland AB, Caty SN, Kabir N, Tapia EE, Trauger SA, Coloma LA, O’Connell LA (2016b) Response to Heethoff, Norton, and Raspotnig: ant and mite diversity drives toxin variation in the little devil poison frog and erratum. J Chem Ecol 42:845–848. https://doi.org/10.1007/s10886-016-0759-y
Miller MA, Schwartz T, Hoover P, Yoshimoto K, Sivagnanam S, Majumdar A (2015) The CIPRES workbench: a flexible framework for creating science gateways. XSEDE '15: Proceedings of the 2015 XSEDE Conference: Scientific advancements enabled by enhanced cyberinfrastructure. 39:1–8. https://doi.org/10.1145/2792745.2792784.
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534. https://doi.org/10.1093/molbev/msaa015
Moritz C, Cicero C (2004) DNA barcoding: promise and pitfalls. PLoS Biol 2:e354. https://doi.org/10.1371/journal.pbio.0020354
Murray EM, Bolton SK, Berg T, Saporito RA (2016) Arthropod predation in a dendrobatid poison frog: does frog life stage matter? Zoology (jena) 119:169–174. https://doi.org/10.1016/j.zool.2016.01.002
Neuwirth M, Daly JW, Myers CW, Tice LW (1979) Morphology of the granular secretory glands in skin of poison-dart frogs (Dendrobatidae). Tissue Cell 11:755–771. https://doi.org/10.1016/0040-8166(79)90029-6
Norton RA, Behan-Pelletier VM (2009) Suborder Oribatida. In: Krantz GW, Walter DE (eds) A manual of acarology, 3rd edn. Texas Tech University Press, Lubbock, pp 430–564
Pachl P, Lindl AC, Krause A, Scheu S, Schaefer I, Maraun M (2019) The tropics as an ancient cradle of oribatid mite diversity. Acarologia 57:309–322. https://doi.org/10.1051/acarologia/20164148
Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Prates I, Paz A, Brown JL, Carnaval AC (2019) Links between prey assemblages and poison frog toxins: A landscape ecology approach to assess how biotic interactions affect species phenotypes. Ecol Evol 9:14317–14329. https://doi.org/10.1002/ece3.5867
Rambaut A (2019) Figtree v1.4.4 http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Raspotnig G (2010) Oil gland secretions in Oribatida (Acari). In: Sabelis MW, Bruin J (eds) Trends in acarology. Springer, Dordrecht, pp 235–239
Raspotnig G, Föttinger P (2008) Analysis of individual oil gland secretion profiles in oribatid mites (Acari: Oribatida). Int J Acarology 34:409–417. https://doi.org/10.1080/17088180809434785
Raspotnig G, Krisper G, Schuster R, Fauler G, Leis HJ (2005) Volatile exudates from the oribatid mite, Platynothrus peltifer. J Chem Ecol 31:419–430. https://doi.org/10.1007/s10886-005-1350-0
Raspotnig G, Leutgeb V, Krisper G, Leis HJ (2011a) Discrimination of Oribotritia species by oil gland chemistry (Acari, Oribatida). Exp Appl Acarol 54:211–224. https://doi.org/10.1007/s10493-011-9434-8
Raspotnig G, Norton RA, Heethoff M (2011b) Oribatid mites and skin alkaloids in poison frogs. Biol Lett 7:555–557. https://doi.org/10.1098/rsbl.2010.1113
Revell LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Santos JC, Cannatella DC (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. Proc Natl Acad Sci U S A 108:6175–6180. https://doi.org/10.1073/pnas.1010952108
Santos JC, Coloma LA, Cannatella DC (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc Natl Acad Sci U S A 100:12792–12797. https://doi.org/10.1073/pnas.2133521100
Saporito RA, Garraffo HM, Donnelly MA, Edwards AL, Longino JT, Daly JW (2004) Formicine ants: An arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc Natl Acad Sci U S A 101:8045–8050. https://doi.org/10.1073/pnas.0402365101
Saporito RA, Donnelly MA, Norton RA, Garraffo HM, Spande TF, Daly JW (2007) Oribatid mites as a major dietary source for alkaloids in poison frogs. Proc Natl Acad Sci U S A 104:8885–8890. https://doi.org/10.1073/pnas.0702851104
Saporito RA, Norton RA, Andriamaharavo NR, Garraffo HM, Spande TF (2011) Alkaloids in the mite Scheloribates laevigatus: further alkaloids common to oribatid mites and poison frogs. J Chem Ecol 37:213–218. https://doi.org/10.1007/s10886-011-9914-7
Saporito RA, Norton RA, Garraffo MH, Spande TF (2015) Taxonomic distribution of defensive alkaloids in Nearctic oribatid mites (Acari, Oribatida). Exp Appl Acarol 67:317–333. https://doi.org/10.1007/s10493-015-9962-8
Savitzky AH, Mori A, Hutchinson DA, Saporito RA, Burghardt GM, Lillywhite HB, Meinwald J (2012) Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22:141–158. https://doi.org/10.1007/s00049-012-0112-z
Schaefer I, Caruso T (2019) Oribatid mites show that soil food web complexity and close aboveground-belowground linkages emerged in the early Paleozoic. Commun Biol 2:387. https://doi.org/10.1038/s42003-019-0628-7
Schatz H, Behan-Pelletier VM, O'Connor BM, Norton RA (2011) Suborder Oribatida van der Hammen, 1968. In: Zhang Z.-Q. (ed) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:141–147.
Schneider K, Maraun M (2005) Feeding preferences among dark pigmented fungal taxa (“Dematiacea”) indicate limited trophic niche differentiation of oribatid mites (Oribatida, Acari). Pedobiologia 49:61–67. https://doi.org/10.1016/j.pedobi.2004.07.010
Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
Sharma PP, Kaluziak ST, Pérez-Porro AR, González VL, Hormiga G, Wheeler WC, Giribet G (2014) Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal. Mol Biol Evol 31:2963–2984. https://doi.org/10.1093/molbev/msu235
Shimano S, Sakata T, Mizutani Y, Kuwahara Y, Aoki J (2002) Geranial: the alarm pheromone in the nymphal stage of the oribatid mite, Nothrus palustris. J Chem Ecol 28:1831–1837. https://doi.org/10.1023/a:1020517319363
Smith KG (2006) Keystone predators (eastern newts, Notophthalmus viridescens) reduce the impacts of an aquatic invasive species. Oecologia 148:342–349. https://doi.org/10.1007/s00442-006-0370-y
Stecher G, Tamura K, Kumar S (2020) Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol 37:1237–1239. https://doi.org/10.1093/molbev/msz312
Stynoski JL, Shelton G, Stynoski P (2014) Maternally derived chemical defences are an effective deterrent against some predators of poison frog tadpoles (Oophaga pumilio). Biol Lett 10:20140187. https://doi.org/10.1098/rsbl.2014.0187
Sullivan J, Swofford DL (2001) Should we use model-based methods for phylogenetic inference when we know that assumptions about among-site rate variation and nucleotide substitution pattern are violated? Syst Biol 50:723–729. https://doi.org/10.1080/106351501753328848
Takada W, Sakata T, Shimano S, Enami Y, Mori N, Nishida R, Kuwahara Y (2005) Scheloribatid mites as the source of pumiliotoxins in dendrobatid frogs. J Chem Ecol 31:2403–2415. https://doi.org/10.1007/s10886-005-7109-9
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035. https://doi.org/10.1073/pnas.0404206101
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tokuyama T, Daly J, Wiktop B (1969) The structure of batrachotoxin, a steroidal alkaloid from the Colombian poison arrow frog, Phyllobates aurotaenia, and partial synthesis of batrachotoxin and its analogs and homologs. J Am Chem Soc 91:3931–3938. https://doi.org/10.1021/ja01042a042
Ujvari B, Casewell NR, Sunagar K, Arbuckle K, Wüster W, Lo N, O’Meally D, Beckmann C, King GF, Deplazes E, Madsen T (2015) Widespread convergence in toxin resistance by predictable molecular evolution. Proc Natl Acad Sci U S A 112:11911–11916. https://doi.org/10.1073/pnas.1511706112
Vaelli PM, Theis KR, Williams JE, O’Connell LA, Foster JA, Eisthen HL (2020) The skin microbiome facilitates adaptive tetrodotoxin production in poisonous newts. eLife 9:e53898. https://doi.org/10.7554/eLife.53898
Vences M, Glaw F, Boehme W (1998) Evolutionary correlates of microphagy in alkaloid-containing frogs (Amphibia: Anura). Zool Anz 236:217–230
Vences M, Schulz S, Poth D, Rodríguez A (2011) Defining frontiers in mite and frog alkaloid research. Biol Lett 7:557. https://doi.org/10.1098/rsbl.2011.0081
Walter DE, Proctor HC (2013) Mites: ecology, evolution & behaviour: Life at a microscale, 2nd edn. Springer Science & Business Media
Weldon PJ, Kramer M, Gordon S, Spande TF, Daly JW (2006) A common pumiliotoxin from poison frogs exhibits enantioselective toxicity against mosquitoes. Proc Natl Acad Sci U S A 103:17818–17821. https://doi.org/10.1073/pnas.0608646103
Weldon PJ, Cardoza YJ, Vander Meer RK, Hoffmann WC, Daly JW, Spande TF (2013) Contact toxicities of anuran skin alkaloids against the fire ant (Solenopsis invicta). Naturwissenschaften 100:185–192. https://doi.org/10.1007/s00114-013-1010-0
Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54:844–851. https://doi.org/10.1080/10635150500354878
Williams BL, Brodie ED Jr, Brodie ED III (2004) A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. J Chem Ecol 30:1901–1919. https://doi.org/10.1023/b:joec.0000045585.77875.09
Wilson EO (2005) Oribatid mite predation by small ants of the genus Pheidole. Insectes Soc 52:263–265. https://doi.org/10.1007/s00040-005-0802-4
Yang L, Ravikanthachari N, Mariño-Pérez R, Deshmukh R, Wu M, Rosenstein A, Kunte K, Song H, Andolfatto P (2019) Predictability in the evolution of orthopteran cardenolide insensitivity. Philos Trans R Soc Lond B Biol Sci 374:20180246. https://doi.org/10.1098/rstb.2018.0246
Young MR, Proctor HC, deWaard JR, Hebert P (2019) DNA barcodes expose unexpected diversity in Canadian mites. Mol Ecol 28:5347–5359. https://doi.org/10.1111/mec.15292
Zimmer RK, Schar DW, Ferrer RP, Krug PJ, Kats LB, Michel WC (2006) The scent of danger: Tetrodotoxin (TTX) as an olfactory cue of predation risk. Ecol Monogr 76:585–600. https://doi.org/10.1890/0012-9615
Zimmer RK, Ferrer RP (2007) Neuroecology, chemical defense, and the keystone species concept. Biol Bull 213:208–225. https://doi.org/10.2307/25066641
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We are grateful to Analisa Shields-Estrada for comments on early versions of the manuscript and to two anonymous reviewers for valuable feedback and comments on an earlier manuscript draft.
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JLC and DCC were supported by a grant from the National Science Foundation (NSF DEB-1556967).
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Coleman, J.L., Cannatella, D.C. How Phylogenetics Can Elucidate the Chemical Ecology of Poison Frogs and Their Arthropod Prey. J Chem Ecol 48, 384–400 (2022). https://doi.org/10.1007/s10886-022-01352-8
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DOI: https://doi.org/10.1007/s10886-022-01352-8