Ecological specialization and reproductive isolation among closely related sympatric ant-eating spiders

. 2022 Sep ; 91 (9) : 1855-1868. [epub] 20220712

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35765936

Grantová podpora
22-20229S Grantová Agentura České Republiky

Biological divergence results from several mechanisms. Defensive mechanisms, such as Batesian mimicry, can cause reproductive isolation via temporal segregation in foraging activity, particularly, in species that closely associate with their model. This seems to be the case of ant-eating spiders, which can be inaccurate Batesian mimics of their prey. Here, we focused on Zodarion nitidum, which has two forms occurring in sympatry, black and yellow. Given the expected noticeable impact of their colour differences on the spiders' interactions with their potential predators and prey, we investigated whether these morphotypes have diverged in other aspects of their biology. We measured the two morphotypes' phenotypic resemblance to a mimetic model, tested whether they were protected from predators, investigated their circadian activity, surveyed the prey they hunted, modelled their distributions, performed crossing experiments and estimated their degree of genetic differentiation. We found that the black morphotype is ant-like, resembling Messor ants, and it was not distinguishable from their ant models by four potential predators. In contrast, the yellow morphotype seems to use predator avoidance as a defensive strategy. Additionally, the two morphotypes differ in their circadian activity, the yellow morphotype being nocturnal and the black one being diurnal. The two morphotypes hunt and associate with different ant prey and possess marked differences in venom composition. Finally, crossing trials showed complete pre-mating isolation between the two morphotypes, but there was no evidence of genetic (mitochondrial data) or environmental niche differentiation. We conclude that the two morphotypes show evidence of a deep differentiation in morphological, behavioural, physiological and ecological traits that evolved together as part of the spider's diverging lifestyles.

Zobrazit více v PubMed

Bennett, A. T., & Théry, M. (2007). Avian color vision and coloration: Multidisciplinary evolutionary biology. The American Naturalist, 169(S1), S1-S6.

Bočánek, O., Šedo, O., Pekár, S., & Zdráhal, Z. (2017). Evaluation of sample preparation protocols for spider venom profiling by MALDI-TOF MS. Toxicon, 133, 18-25.

Brown, P. E., Frank, C. P., Groves, H. L., & Anderson, M. (1998). Spectral sensitivity and visual conditioning in the parasitoid wasp Trybliographa rapae (Hymenoptera: Cynipidae). Bulletin of Entomological Research, 88(3), 239-245.

Čandek, K., & Kuntner, M. (2014). DNA barcoding gap: Reliable species identification over morphological and geographical scales. Molecular Ecology Resources, 15, 268-277.

Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772.

De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879-886.

Defrize, J., Théry, M., & Casas, J. (2010). Background colour matching by a crab spider in the field: A community sensory ecology perspective. Journal of Experimental Biology, 213(9), 1425-1435.

Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302-4315. https://doi.org/10.1002/joc.5086

Fleishman, L. J., Perez, C. W., Yeo, A. I., Cummings, K. J., Dick, S., & Almonte, E. (2016). Perceptual distance between colored stimuli in the lizard Anolis sagrei: Comparing visual system models to empirical results. Behavioral Ecology and Sociobiology, 70(4), 541-555.

Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase sub- unit I from diverse metazoan invertebrates. Molecular Marine Biology Biotechnology, 3(5), 294-299.

Funk, D. J., & Omland, K. E. (2003). Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34, 397-423.

Harkness, M. L. R., & Harkness, R. D. (1992). Predation of an ant (Cataglyphis bicolor [F.] Hym., Formicidae) by a spider (Zodarium frenatum (Simon) Araneae, Zodariidae) in Greece. Entomologist's Monthly Magazine, 128, 147-156.

Hedin, M. C., & Maddison, W. P. (2001). A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Molecular Phylogenetics and Evolution, 18, 386-403.

Hijmans, R. J. & Etten, R.V. (2012). raster: Geographic analysis and modeling with raster data. R package version 2.0-12. Retrieved from http://CRAN.R-project.org/package=raster

Hoskin, C. J., & Higgie, M. (2010). Speciation via species interactions: The divergence of mating traits within species. Ecology Letters, 13, 409-420.

I de Lanuza, G. P., Ábalos, J., Bartolomé, A., & Font, E. (2018). Through the eye of a lizard: Hue discrimination in a lizard with ventral polymorphic coloration. Journal of Experimental Biology, 221(5), jeb169565.

Ivanov, V., Lee, K. M., & Mutanen, M. (2018). Mitonuclear discordance in wolf spiders: Genomic evidence for species integrity and introgression. Molecular Ecology, 27, 1681-1695.

Ježek, J. (2015). Similarity measurement of spiders and ants (Master thesis). Masaryk University.

Jiggins, C. D. (2008). Ecological speciation in mimetic butterflies. Bioscience, 58(6), 541-548.

Jiggins, C. D., Emelianov, I., & Mallet, J. (2005). Assortative mating and speciation as pleiotropic effects of ecological adaptation: Examples in moths and butterflies. In M. D. E. Fellows, G. J. Holloway, & J. Folff (Eds.), Insect evolutionary ecology (pp. 455-478). CABI Publishing.

Kazemi, B., Gamberale-Stille, G., Tullberg, B. S., & Leimar, O. (2014). Stimulus salience as an explanation for imperfect mimicry. Current Biology, 24(9), 965-969.

Knowles, L. L., & Carstens, B. C. (2007). Delimiting species without monophyletic gene trees. Systematic Biology, 56, 887-895.

Kozlov, A. M., Darriba, D., Flouri, T., Morel, B., & Stamatakis, A. (2019). RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics, 35, 4453-4455.

Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.

Lattimore, V. L., Vink, C. J., Paterson, A. M., & Cruickshank, R. H. (2011). Unidirectional introgression within the genus Dolomedes (Araneae:Pisauridae) in southern New Zealand. Invertebrate Systematics, 25, 70-79.

Lazareva, O. F., Vecera, S. P., Levin, J., & Wasserman, E. A. (2005). Object discrimination by pigeons: Effects of object color and shape. Behavioural Processes, 69(1), 17-31.

Levy, G. (1992). The spider genera Palaestina, Trygetus, Zodarion and Ranops (Araneae, Zodariidae) in Israel with annotations on species of the Middle East. Israel Journal of Zoology, 38(2), 67-110.

Maddison, W. P., & Maddison, D. R. (2019). Mesquite: A modular system for evolutionary analysis. Version 3.61. Retrieved from http://www.mesquiteproject.org

Maia, R., Eliason, C. M., Bitton, P.-P., Doucet, S. M., & Shawkey, M. D. (2013). pavo: An R Package for the analysis, visualization and organization of spectral data. Methods in Ecology and Evolution, 4(10), 609-613.

Martin, M., Le Galliard, J. F., Meylan, S., & Loew, E. R. (2015). The importance of ultraviolet and near-infrared sensitivity for visual discrimination in two species of lacertid lizards. Journal of Experimental Biology, 218(3), 458-465.

Martišová, M., Bilde, T., & Pekár, S. (2009). Sex-specific kleptoparasitic foraging in ant-eating spiders. Animal Behaviour, 78(5), 1115-1118.

McKay, B. D., & Zink, R. M. (2010). The causes of mitochondrial DNA gene tree paraphyly in birds. Molecular Phylogenetics and Evolution, 54, 647-650.

Michálek, O., Kuhn-Nentwig, L., & Pekár, S. (2019). High specific efficiency of venom of two prey-specialized spiders. Toxins, 11(12), 687.

Muscarella, R., Galante, P. J., Soley-Guardia, M., Boria, R. A., Kass, J. M., Uriarte, M., & Anderson, R. P. (2014). ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution, 5(11), 1198-1205.

Nelson, X. J. (2012). A predator's perspective of the accuracy of ant mimicry in spiders. Psyche, 2012, 168549, 1, 5.

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E. & Wagner, H. (2016). Vegan: Community ecology package. R package version 2.3-5. Retrieved from https://CRAN.R-project.org/package=vegan

Ortiz, D., & Francke, O. F. (2015). Two new species of Bonnetina tarantulas (Theraphosidae: Theraphosinae) from Mexico: Contributions to morphological nomenclature and molecular characterization of types. Journal of Natural History, 49, 685-707.

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. Molecular Phylogenetics and Evolution, 154, 106997.

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.

Pekár, S. (2004). Predatory behavior of two European ant-eating spiders (Araneae, Zodariidae). Journal of Arachnology, 32(1), 31-41.

Pekár, S. (2014). Is inaccurate mimicry ancestral to accurate in myrmecomorphic spiders (Araneae)? Biological Journal of the Linnean Society, 113, 97-111.

Pekár, S. (2022). New drivers of the evolution of mimetic accuracy in Batesian ant-mimics: Size, habitat and latitude. Journal of Biogeography, 49, 14-21.

Pekár, S., & Brabec, M. (2016). Modern Analysis of Biological Data. Generalised Linear Models in R. Masaryk University Press.

Pekár, S., & Jarab, M. (2011). Assessment of color and behavioral resemblance to models by inaccurate myrmecomorphic spiders (Araneae). Invertebrate Biology, 130(1), 83-90.

Pekár, S., Jarab, M., Fromhage, L., & Herberstein, M. E. (2011). Is the evolution of innacurate mimicry a result of selection by a suit of predators? A case study using myrmecomorphic spiders. The American Naturalist, 178(1), 124-134.

Pekár, S., & Král, J. (2001). A comparative study of the biology and karyotypes of two central European zodariid spiders (Araneae, Zodariidae). Journal of Arachnology, 29(3), 345-353.

Pekár, S., & Král, J. (2002). Mimicry complex in two central European zodariid spiders (Araneae: Zodariidae): How Zodarion deceives ants. Biological Journal of the Linnean Society, 75(4), 517-532.

Pekár, S., Král, J., & Lubin, Y. D. (2005). Natural history and karyotype of some ant-eating zodariid spiders (Araneae, Zodariidae) from Israel. Journal of Arachnology, 33, 50-62.

Pekár, S., Líznarová, E., Bočánek, O., & Zdráhal, Z. (2018). Venom of prey-specialised spiders is more toxic to their preferred prey: A result of prey-specific toxins. Journal of Animal Ecology, 87, 1639-1652.

Pekár, S., & Lubin, Y. (2003). Habitats and interspecific associations of zodariid spiders in the Negev (Araneae: Zodariidae). Israel Journal of Zoology, 49(4), 255-267.

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). Molecular Ecology, 27(4), 1053-1064.

Pekár, S., Šedo, O., Líznarová, E., Korenko, S., & Zdráhal, Z. (2014). David and the Goliath: Potent venom of an ant-eating spider (Araneae) enables capture of a giant prey. Naturwissenschaften, 101(7), 533-540.

Pekár, S., Sentenská L., & Šedo, O. (2022). Data on Zodarion nitidum morphotypes. Masaryk University, https://doi.org/10.57758/0p0v-gj43

Pekár, S., Šmerda, J., Hrušková, M., Šedo, O., Muster, C., Cardoso, P., Zdráhal, Z., Korenko, S., Bureš, P., Líznarová, E. & Sentenská, L. (2012). Prey-race drives differentiation of biotypes in ant-eating spiders. Journal of Animal Ecology, 81(4), 838-848.

Pekár, S., Toft, S., Hrušková, M., & Mayntz, D. (2008). Dietary and prey-capture adaptations by which Zodarion germanicum, an ant-eating spider (Araneae: Zodariidae), specialises on the Formicinae. Naturwissenschaften, 95(3), 233-239.

Pekár, S., Tsai, Y.-Y., & Michalko, R. (2020). Transformational mimicry in a myrmecomorphic spider. The American Naturalist, 196(2), 216-226.

Pekár, S., Wolff, J., Černecká, Ľ., Birkhofer, K., Mammola, S., Lowe, E. C., Fukushima, C. S., Herberstein, M. E., Kučera, A., Buzatto, B., Djoudi, E. A., Domenech, M., Enciso, A. V., Piñanez Espejo, Y. M. G., Febles, S., García, L. F., Gonçalves-Souza, T., Isaia, M., Lafage, D., … Cardoso, P. (2021). The World Spider Trait database: A centralised global open repository for curated data on spider traits. Database, 2021, baab064.

Pfennig, D. W., Akcali, C. K., & Kikuchi, D. W. (2015). Batesian mimicry promotes pre-and postmating isolation in a snake mimicry complex. Evolution, 69(4), 1085-1090.

Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231-259.

R Core Team. (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901-904.

Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.

Ruxton, G. D., Allen, W. L., Sherratt, T. N., & Speed, M. P. (2019). Avoiding attack: The evolutionary ecology of crypsis, aposematism, and mimicry. Oxford University Press.

Schaefer, M. H., Schaefer, V., & Vorobyev, M. (2007). Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals? The American Naturalist, 169(S1), S159-S169.

Schoener, T. W. (1968). The Anolis lizards of Bimini: Resource partitioning in a complex fauna. Ecology, 49, 704-726.

Sontag, C. (1971). Spectral sensitivity studies on the visual system of the praying mantis, Tenodera sinensis. Journal of General Physiology, 57(1), 93-112.

Toews, D. P. L., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907-3930.

Vassilevski, A. A., Kozlov, S. A., & Grishin, E. V. (2009). Molecular diversity of spider venom. Biochemistry, 74(13), 1505-1534.

Veselý, P., Dobrovodský, J., & Fuchs, R. (2021). Predation by avian predators may have initiated the evolution of myrmecomorph spiders. Scientific Reports, 11(1), 1-8.

Vorobyev, M., Osorio, D., Bennett, A., Marshall, N., & Cuthill, I. (1998). Tetrachromacy, oil droplets and bird plumage colours. Journal of Comparative Physiology A - Neuroethology Sensory Neural and Behavioral Physiology, 183(5), 621-633.

Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche identity versus conservatism: Quantitative approaches to niche evolution. Evolution, 62, 2868-2883.

Warren, D. L., Matzke, N., Cardillo, M., Baumgartner, J., Beaumont, L., Huron, N., Simões, M., & Dinnage, R. (2019). ENMTools (Software package). Retrieved from https://github.com/danlwarren/ENMTools

Warren, D. L., & Seifert, S. N. (2011). Ecological niche modeling in Maxent: The importance of model complexity and the performance of model selection criteria. Ecological Applications, 21, 335-342.

Wheeler, B., & Torchiano, M. (2016). lmPerm: Permutation tests for linear models. R package version 2.1.0. Retrieved from https://CRAN.R-project.org/package=lmPerm

Wood, S. N. (2006). Generalized additive models: An introduction with R. Chapman and Hall/CRC.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Dynamic evolution of size and colour in the highly specialized Zodarion ant-eating spiders

. 2023 Aug 09 ; 290 (2004) : 20230797. [epub] 20230809

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...