Dynamic evolution of size and colour in the highly specialized Zodarion ant-eating spiders
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37554037
PubMed Central
PMC10410226
DOI
10.1098/rspb.2023.0797
Knihovny.cz E-zdroje
- Klíčová slova
- hyRAD sequencing, mimicry, morphological evolution, museomics, phylogenomics, prey shift,
- MeSH
- barva MeSH
- fylogeneze MeSH
- genomika MeSH
- pavouci * genetika MeSH
- predátorské chování MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Ecological specialists constitute relevant case studies for understanding the mechanisms, potential and limitations of evolution. The species-rich and strictly myrmecophagous spiders of the genus Zodarion show diversified defence mechanisms, including myrmecomorphy of different ant species and nocturnality. Through Hybridization Capture Using RAD Probes (hyRAD), a phylogenomic technique designed for sequencing poorly preserved specimens, we reconstructed a phylogeny of Zodarion using 52 (approx. a third of the nominal) species that cover its phylogenetic and distributional diversity. We then estimated the evolution of body size and colour, traits that have diversified noticeably and are linked to defence mechanisms, across the group. Our genomic matrix of 300 loci led to a well-supported phylogenetic hypothesis that uncovered two main clades inside Zodarion. Ancestral state estimation revealed the highly dynamic evolution of body size and colour across the group, with multiple transitions and convergences in both traits, which we propose is likely indicative of multiple transitions in ant specialization across the genus. Our study will allow the informed targeted selection of Zodarion taxa of special interest for research into the group's remarkable adaptations to ant specialization. It also exemplifies the utility of hyRAD for phylogenetic studies using museum material.
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
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Thompson JN. 1994. The coevolutionary process. Chicago, IL: The University of Chicago Press. (10.7208/chicago/9780226797670.001.0001) DOI
Schluter D. 2000. The ecology of adaptive radiation. New York, NY: Oxford University Press.
Natural History Museum of Bern. 2023. World Spider Catalog. Version 24. See https://wsc.nmbe.ch.
Pekár S, Toft S. 2015. Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol. Rev. 90, 744-761. (10.1111/brv.12133) PubMed DOI
Michálek O, Kuhn-Nentwig L, Pekár S. 2019. High specific efficiency of venom of two prey-specialized spiders. Toxins (Basel) 11, 687. (10.3390/toxins11120687) PubMed DOI PMC
Pekár S, Petráková L, Šedo O, Korenko S, Zdráhal Z. 2018. Trophic niche, capture efficiency and venom profiles of six sympatric ant-eating spider species (Araneae: Zodariidae). Mol. Ecol. 27, 1053-1064. (10.1111/mec.14485) PubMed DOI
Pekár S, Král J, Lubin Y. 2005. Natural history and karyotype of some ant-eating zodariid spiders (Araneae, Zodariidae) from Israel. J. Arachnol. 33, 50-62. (10.1636/S03-2) DOI
Pekár S, Jarab M. 2011. Assessment of color and behavioral resemblance to models by inaccurate myrmecomorphic spiders (Araneae). Invertebr. Biol. 130, 83-90. (10.1111/j.1744-7410.2010.00217.x) DOI
Pekár S, Martišová M, Tóthová AŠ, Haddad CR. 2022. Mimetic accuracy and coevolution of mimetic traits in ant-mimicking species. iScience 25, 105126. (10.1016/j.isci.2022.105126) PubMed DOI PMC
Pekár S, Ortiz D, Sentenská L, Šedo O. 2022. Ecological specialization and reproductive isolation among closely related sympatric ant-eating spiders. J. Anim. Ecol. 91, 1855-1868. (10.1111/1365-2656.13767) PubMed DOI
Pekár S, et al. 2012. Prey-race drives differentiation of biotypes in ant-eating spiders. J. Anim. Ecol. 81, 838-848. (10.1111/j.1365-2656.2012.01957.x) PubMed DOI
Ortiz D, Petráková Dušátková L, Pekár S. 2022. Gut content metabarcoding of three widespread Iberian ant-eating spiders reveals specialisation on the same abundant harvester ants. Ecol. Entomol. 47, 305-313. (10.1111/een.13114) DOI
Ortiz D, Pekár S, Dianat M. 2022. Phylogenomics and loci dropout patterns of deeply diverged Zodarion ant-eating spiders suggest a high potential of RAD-seq for genus-level spider phylogenetics. Cladistics 38, 320-334. (10.1111/cla.12493) PubMed DOI
Bosmans R. 1994. Revision of the genus Zodarion Walckenaer, 1833 in the Iberian Peninsula and Balearic Islands (Araneae, Zodariidae). Eos (Washington. DC) 69, 115-142.
Bosmans R. 1997. Revision of the genus Zodarion Walckenaer, 1833, part II. Western and Central Europe, including Italy (Araneae: Zodariidae). Bull. Br. arachnol.Soc. 10, 265-294.
Suchan T, Pitteloud C, Gerasimova NS, Kostikova A, Schmid S, Arrigo N, Pajkovic M, Ronikier M, Alvarez N. 2016. Hybridization Capture Using RAD Probes (hyRAD), a new tool for performing genomic analyses on collection specimens. PLoS ONE 11, e0151651. (10.1371/journal.pone.0151651) PubMed DOI PMC
Bosmans R. 2009. Revision of the genus Zodarion Walckenaer, 1833, part III. South East Europe and Turkey (Araneae: Zodariidae). Contrib. Nat. Hist. 12, 211-295.
Levy G. 1992. The spider genera Palaestina, Trygetus, Zodarion and Ranops (Araneae, Zodariidae) in Israel with annotations on species of the Middle East. Isr. J. Zool. 38, 67-110.
Benhalima S, Bosmans R. 2020. Revision of the genus Zodarion Walckenaer, 1833 (part IV). The species of Morocco (Araneae: Zodariidae). Zootaxa 4899, 93-114. (10.11646/zootaxa.4899.1.5) PubMed DOI
Toussaint EFA, Gauthier J, Bilat J, Gillett CPDT, Gough HM, Lundkvist H, Blanc M, Muñoz-Ramírez CP, Alvarez N. 2021. HyRAD-X exome capture museomics unravels giant ground beetle evolution. Genome Biol. Evol. 13, evab112. (10.1093/gbe/evab112) PubMed DOI PMC
Eaton DAR, Overcast I. 2020. ipyrad: interactive assembly and analysis of RADseq datasets. Bioinformatics 36, 2592-2594. (10.1093/bioinformatics/btz966) PubMed DOI
Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. (https://arxiv.org/abs/1303.3997)
R Core Team.2022. R: a language and environment for statistical computing. Version 4.2.1. Vienna, Austria: R Foundation for Statistical Computing.
Borowiec ML. 2016. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4, e1660. (10.7717/peerj.1660) PubMed DOI PMC
Jocqué R. 1991. A generic revision of the spider family Zodariidae (Araneae). Bull. Am. Museum Nat. Hist. 201, 1-160.
Henrard A. 2019. Systematics and phylogeny of the ant-eating spiders (Araneae; Zodariidae): a total evidence analysis. PhD thesis, Université Catholique de Louvain, Leuven, Belgium.
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. (10.1093/molbev/msaa015) PubMed DOI PMC
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. (10.1038/nmeth.4285) PubMed DOI PMC
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518-522. (10.1093/molbev/msx281) PubMed DOI PMC
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. (10.1093/sysbio/syq010) PubMed DOI
Aberer AJ, Krompass D, Stamatakis A. 2013. Pruning rogue taxa improves phylogenetic accuracy: an efficient algorithm and webservice. Syst. Biol. 62, 162-166. (10.1093/sysbio/sys078) PubMed DOI PMC
Aberer AJ, Kobert K, Stamatakis A. 2014. ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31, 2553-2556. (10.1093/molbev/msu236) PubMed DOI PMC
Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinf. 19, 15-30. (10.1186/s12859-018-2129-y) PubMed DOI PMC
Morel B, Kozlov AM, Stamatakis A. 2019. ParGenes: a tool for massively parallel model selection and phylogenetic tree inference on thousands of genes. Bioinformatics 35, 1771-1773. (10.1093/bioinformatics/bty839) PubMed DOI PMC
Junier T, Zdobnov EM. 2010. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 26, 1669-1670. (10.1093/bioinformatics/btq243) PubMed DOI PMC
Sayyari E, Mirarab S. 2016. Fast coalescent-based computation of local branch support from quartet frequencies. Mol. Biol. Evol. 33, 1654-1668. (10.1093/molbev/msw079) PubMed DOI PMC
Chifman J, Kubatko L. 2014. Quartet inference from SNP data under the coalescent model. Bioinformatics 30, 3317-3324. (10.1093/bioinformatics/btu530) PubMed DOI PMC
Swofford DL. 2019. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. See https://paup.phylosolutions.com.
Minh BQ, Hahn MW, Lanfear R. 2020. New methods to calculate concordance factors for phylogenomic datasets. Mol. Biol. Evol. 37, 2727-2733. (10.1093/molbev/msaa106) PubMed DOI PMC
Paradis E, Schliep K. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526-528. (10.1093/bioinformatics/bty633) PubMed DOI
Revell LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (10.1111/j.2041-210X.2011.00169.x) DOI
Pennell MW, Eastman JM, Slater GJ, Brown JW, Uyeda JC, FitzJohn RG, Alfaro ME, Harmon LJ. 2014. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216-2218. (10.1093/bioinformatics/btu181) PubMed DOI
Ortiz D, Pekár S, Bilat J, Alvarez N. 2021. Poor performance of DNA barcoding and the impact of RAD loci filtering on the species delimitation of an Iberian ant-eating spider. Mol. Phylogenet. Evol. 154, 106997. (10.1016/j.ympev.2020.106997) PubMed DOI
Schmid S, Neuenschwander S, Pitteloud C, Heckel G, Pajkovic M, Arlettaz R, Alvarez N. 2018. Spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus revealed by museum genomics. Ecol. Evol. 8, 1480-1495. (10.1002/ece3.3699) PubMed DOI PMC
Gauthier J, Pajkovic M, Neuenschwander S, Kaila L, Schmid S, Orlando L, Alvarez N. 2020. Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland. Mol. Ecol. Resour. 20, 1191-1205. (10.1111/1755-0998.13167) PubMed DOI PMC
Schmid S, Genevest R, Gobet E, Suchan T, Sperisen C, Tinner W, Alvarez N. 2017. HyRAD-X, a versatile method combining exome capture and RAD sequencing to extract genomic information from ancient DNA. Methods Ecol. Evol. 8, 1374-1388. (10.1111/2041-210X.12785) DOI
Palmer M, et al. 2019. The synergistic effect of concatenation in phylogenomics: the case in Pantoea. PeerJ 7, e6698. (10.7717/peerj.6698) PubMed DOI PMC
Gatesy J, Springer MS. 2014. Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum. Mol. Phylogenet. Evol. 80, 231-266. (10.1016/j.ympev.2014.08.013) PubMed DOI
Mirarab S, Bayzid MS, Warnow T. 2016. Evaluating summary methods for multilocus species tree estimation in the presence of incomplete lineage sorting. Syst. Biol. 65, 366-380. (10.1093/sysbio/syu063) PubMed DOI
Kubatko LS, Degnan JH. 2007. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56, 17-24. (10.1080/10635150601146041) PubMed DOI
Prüfer K, Stenzel U, Hofreiter M, Pääbo S, Kelso J, Green RE. 2010. Computational challenges in the analysis of ancient DNA. Genome Biol. 11, R47. (10.1186/gb-2010-11-5-r47) PubMed DOI PMC
Maddison WP. 1997. Gene trees in species trees. Syst. Biol. 46, 523-536. (10.1017/CBO9781107415324.004) DOI
Mallet J. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229-237. (10.1016/j.tree.2005.02.010) PubMed DOI
Wolff JO, Wierucka K, Uhl G, Herberstein ME. 2021. Building behavior does not drive rates of phenotypic evolution in spiders. Proc. Natl Acad. Sci. USA 118, 9-11. (10.1073/pnas.2102693118) PubMed DOI PMC
Wolff JO, Wierucka K, Paterno GB, Coddington JA, Hormiga G, Kelly MBJ, Herberstein ME, Ramírez MJ. 2022. Stabilized morphological evolution of spiders despite mosaic changes in foraging ecology. Syst. Biol. 71, 1487-1503. (10.1093/sysbio/syac023) PubMed DOI
Kuntner M, et al. 2019. Golden orbweavers ignore biological rules: phylogenomic and comparative analyses unravel a complex evolution of sexual size dimorphism. Syst. Biol. 68, 555-572. (10.1093/sysbio/syy082) PubMed DOI PMC
Cheng R-C, Kuntner M. 2014. Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders. Evolution 68, 2861-2872. (10.1111/evo.12504) PubMed DOI
Landis MJ, Schraiber JG. 2017. Pulsed evolution shaped modern vertebrate body sizes. Proc. Natl Acad. Sci. USA 114, 13 224-13 229. (10.1073/pnas.1710920114) PubMed DOI PMC
Girard MB, Elias DO, Kasumovic MM. 2015. Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders. Proc. R. Soc. B 282, 20152222. (10.1098/rspb.2015.2222) PubMed DOI PMC
Entling W, Schmidt-Entling MH, Bacher S, Brandl R, Nentwig W. 2010. Body size-climate relationships of European spiders. J. Biogeogr. 37, 477-485. (10.1111/j.1365-2699.2009.02216.x) DOI
Grinsted L, Schou MF, Settepani V, Holm C, Bird TL, Bilde T. 2020. Prey to predator body size ratio in the evolution of cooperative hunting—a social spider test case. Dev. Genes Evol. 230, 173-184. (10.1007/s00427-019-00640-w) PubMed DOI
Gillespie RG, Benjamin SP, Brewer MS, Rivera MAJ, Roderick GK. 2018. Repeated diversification of ecomorphs in Hawaiian stick spiders. Curr. Biol. 28, 941-947.e3. (10.1016/j.cub.2018.01.083) PubMed DOI
Rosenblum EB, Parent CE, Diepeveen ET, Noss C, Bi K. 2017. Convergent phenotypic evolution despite contrasting demographic histories in the fauna of White Sands. Am. Nat. 190, S44-S56. (10.1086/692138) PubMed DOI
Foley S, Saranathan V, Piel WH. 2020. The evolution of coloration and opsins in tarantulas. Proc. R. Soc. B 287, 20201688. (10.1098/rspb.2020.1688) PubMed DOI PMC
McIver J, Gary S. 1993. Myrmecomorphy: morphological and behavioral mimicry of ants. Annu. Rev. Entomol. 38, 351-380. (10.1146/annurev.ento.38.1.351) DOI
Pekár S, Petráková L, Corcobado G, Whyte R. 2017. Revision of eastern Australian ant-mimicking spiders of the genus Myrmarachne (Araneae, Salticidae) reveals a complex of species and forms. Zool. J. Linn. Soc. 179, 642-676. (https://academic.oup.com/zoolinnean/article/179/3/642/3058146)
Ortiz D, Pekár S, Bilat J, Shafaie S, Alvarez N, Gauthier J. 2023. Dynamic evolution of size and colour in the highly specialized Zodarion ant-eating spiders. Figshare. (10.6084/m9.figshare.c.6753818) PubMed DOI PMC
Dynamic evolution of size and colour in the highly specialized Zodarion ant-eating spiders
figshare
10.6084/m9.figshare.c.6753818