Abstract
Sexual size dimorphism in orb-weaving spiders is a relatively well-studied phenomenon, and numerous works have documented evolutionary variation in interspecific size and degree of dimorphism. To date, these studies have been largely limited to assessing the evolution of a single or few linear measurements correlated with body size. While the descriptive and comparative literature is rich with qualitative and linear comparisons that distinguish the sexes and characterize species, the extent to which interspecific or dimorphic variation in size correlates with morphological shape remains relatively unexplored. The carapace of spiders is generally conserved in shape, especially among members of the same family, but is neither well-characterized as a potential facet of spider sexual dimorphism nor as a variable structure overall. Here, we use geometric morphometric techniques to quantify differences in carapace shape among members of the family Araneidae and test for allometric influences on interspecific and dimorphic shape differences across orb-weavers. We show that females and males differ in shape, occupying overlapping but distinct areas of morphospace, with males having more piriform carapaces than females. Araneid spider subfamilies overlap substantially in morphospace, though interspecific differences in shape are generally greater than those distinguishing males and females of a species. Furthermore, we show that female carapace shape shows phylogenetic signal and is more conserved than is male shape. Carapace shape differences made evident from canonical variates analysis are congruent with the more mobile lifestyle adopted by males, as a broader carapace may support more robust leg musculature.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abouheif, E., & Fairbairn, D. J. (1997). A comparative analysis of allometry for sexual size dimorphism: Assessing Rensch’s rule. The American Naturalist, 149, 540–562.
Adams, D.C., Collyer, M., & Kaliontzopoulou, A. (2018). Geomorph: Software for geometric morphometric analysis. R package version 3.0.6. https://cran.r-project.org/package=geomorph.
Adams, D. C., & Otárola-Castillo, E. (2013). Geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399. https://doi.org/10.1111/2041-210X.12035.
Blomberg, S. P., Garland, T., Jr., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.
Bond, J. E., & Beamer, D. A. (2006). A morphometric analysis of mygalomorph spider carapace shape and its efficacy as a phylogenetic character. Invertebrate Systematics, 20, 1–7.
Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. New York: Cambridge University Press.
Brandt, Y., & Andrade, M. C. B. (2007a). Testing the gravity hypothesis of sexual size dimorphism: Are small males faster climbers? Functional Ecology, 21, 379–385. https://doi.org/10.1111/j.1365-2435.2007.01243.x.
Brandt, Y., & Andrade, M. C. B. (2007). What is the matter with the gravity hypothesis? Functional Ecology, 21, 1182–1183. https://doi.org/10.1111/j.1365-2435.2007.01345.x.
Cardini, A. (2016). Lost in the other half: Improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Systematic Biology, 65, 1096–1106. https://doi.org/10.1093/sysbio/syw043.
Cardini, A. (2017). Left, right, or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. Journal of Zoological Systematics and Evolutionary Research, 55, 1–10. https://doi.org/10.1111/jzs.12144.
Costa-Schmidt, L. E., & de Araujo, A. M. (2010). Genitalic variation and taxonomic discrimination in the semi-aquatic spider genus Paratrechalea (Araneae: Trechaleidae). Journal of Arachnology, 38, 242–249.
Cheng, R. C., & Kuntner, M. (2014). Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders. Evolution, 68(10), 2861–2872. https://doi.org/10.1111/evo.12504.
Cheng, R. C., & Kuntner, M. (2015). Disentangling the size and shape components of sexual dimorphism. Journal of Evolutionary Biology, 42, 223–234. https://doi.org/10.1007/s11692-015-9313-z.
Coddington, J. A. (1986). The genera of the spider family Theridiosomatidae. Smithsonian Contributions to Zoology, 4422, 1–96.
Collyer, M. L., & Adams, D. C. (2018). RRPP: An R package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution, 9, 1772–1779. https://doi.org/10.1111/2041-210X.13029.
Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity, 115, 357–365. https://doi.org/10.1038/hdy.2014.75.
Corcobado, G., Rodríguez-Gironés, M. A., De Mas, E., & Moya-Laraño, J. (2010). Introducing the refined gravity hypothesis of extreme sexual size dimorphism. BMC Evolutionary Biology, 10, 236. https://doi.org/10.1186/1471-2148-10-236.
Crews, S. C. (2009). Assessment of rampant genitalic variation in the spider genus Homalonychus (Araneae, Homalonychidae). Invertebrate Biology, 128, 107–125.
Darwin, C. (1871). Sexual selection and the descent of man. London: Murray.
De Mas, E., Ribera, C., & Moya-Laraño, J. (2009). Resurrecting the differential mortality model of sexual size dimorphism. Journal of Evolutionary Biology, 22, 1739–1749. https://doi.org/10.1111/j.1420-9101.2009.01786.x.
Dimitrov, D., Benavides, L. R., Arnedo, M. A., Giribet, G., Griswold, C. E., Scharff, N., et al. (2017). Rounding up the usual suspects: A standard target-gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb-weaving spiders with a new family-rank classification (Araneae, Araneoidea). Cladistics, 33, 221–250. https://doi.org/10.1111/cla.12165.
Drake, A. G., & Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. The American Naturalist, 175, 289–301. https://doi.org/10.1086/650372.
Eberhard, W. G., Huber, B. A., Rodriguez-S, R. L., Briceño, R. D., Salas, I., & Rodriguez, V. (1998). One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution, 52, 415–431. https://doi.org/10.1111/j.1558-5646.1998.tb01642.x.
Elgar, M. A. (1998). Sperm competition and sexual selection in spiders and other arachnids. In T. R. Birkhead & A. P. Møller (Eds.), Sperm competition and sexual selection (pp. 3073–3140). London: Academic Press.
Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15.
Fernández-Montraveta, C., & Marugán-Lobón, J. (2017). Geometric morphometrics reveals sex-differential shape allometry in a spider. PeerJ, 5, e3617. https://doi.org/10.7717/peerj.3617.
Fernández, R., Kallal, R. J., Dimitrov, D., Ballesteros, J. A., Arnedo, M. A., Giribet, G., et al. (2018). Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life. Current Biology, 28, 2190–2193. https://doi.org/10.1016/j.cub.2018.03.064.
Foelix, R. F. (2010). Biology of spiders (3rd ed.). New York: Oxford University Press.
Foellmer, M. W., & Fairbairn, D. J. (2005). Selection on male size, leg length and condition during mate search in a sexually highly dimorphic orb-weaving spider. Oecologia, 142, 653–662. https://doi.org/10.1007/s00442-004-1756-3.
Foellmer, M. W., & Moya-Laraño, J. (2007). Sexual size dimorphism in spiders: Patterns and processes. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Szekely (Eds.), Sex, size and gender roles: evolutionary studies of sexual size dimorphism (pp. 71–81). New York: Oxford University Press.
Garrison, N. L., Rodriguez, J., Agnarsson, I., Coddington, J. A., Griswold, C. E., Hamilton, C. A., et al. (2016). Spider phylogenomics: Untangling the spider tree of life. PeerJ, 4, e1719. https://doi.org/10.7717/peerj.1719.
Gelman, A., & Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science, 7, 457–472.
Gertsch, W. J. (1955). The North American bolas spiders of the genera Mastophora and Agatostichus. Bulletin of the American Museum of Natural History, 106, 225–254.
Gower, J. C. (1975). Generalized Procrustes analysis. Psychometrika, 40, 33–51.
Gregorič, M., Agnarsson, I., Blackledge, T. A., & Kuntner, M. (2015). Phylogenetic position and composition of Zygiellinae and Caerostris, with new insight into orb-web evolution and gigantism. Zoological Journal of the Linnean Society, 175, 225–243. https://doi.org/10.1111/zoj.12281.
Grossi, B., & Canals, M. (2015). Energetics, scaling, and sexual size dimorphism of spiders. Acta Biotheoretica, 63, 71–81. https://doi.org/10.1007/s10441-014-9237-5.
Grossi, B., Veloso, C., Taucare-Ríos, A., & Canals, M. (2016). Allometry of locomotor organs and sexual size dimorphism in the mygalomorph spider Grammostola rosea (Walckenaer, 1837) (Araneae, Theraphosidae). Journal of Arachnology, 44, 99–102.
Guillerme, T. (2018). dispRity: A modular R package for measuring disparity. Methods in Ecology and Evolution, 9, 1755–1763.
Guillerme, T., & Cooper, N. (2018). dispRity manual. https://doi.org/10.6084/m9.figshare.6187337.v1.
Gunz, P., & Mitteroecker, P. (2013). Semilandmarks: A method for quantifying curves and surfaces. Hystrix, 24, 103–109. https://doi.org/10.4404/hystrix-24.1-6292.
Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Kluwer Academic.
Hammer, Ø., Harper, D.A.T., & Ryan, P.D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, (1): 9. https://palaeo-electronica.org/2001_1/past/issue1_01.htm
Hansen, T. F. (1997). Stabilizing selection and the comparative analyses of adaptation. Evolution, 51, 1341–1351. https://doi.org/10.1111/j.1558-5646.1997.tb01457.x.
Head, G. (1995). Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (Class Araneae). Evolution, 49, 776–781.
Hopkins, M. J., & Gerber, S. (2017). Morphological disparity. Cham: Springer.
Hormiga, G., Scharff, N., & Coddington, J. A. (2000). The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Systematic Biology, 49, 435–462.
Kallal, R. J., Dimitrov, D., Arnedo, M. A., Giribet, G., & Hormiga, G. (2019). Monophyly, taxon sampling, and the nature of ranks in the classification of orb-weaving spiders (Araneae: Araneoidea). Systematic Biology. https://doi.org/10.1093/sysbio/syz043.
Kallal, R. J., Fernández, R., Giribet, G., & Hormiga, G. (2018). A phylotranscriptomic backbone of the orb-weaving spider family Araneidae (Arachnida, Araneae) supported by multiple methodological approaches. Molecular Phylogenetics and Evolution, 126, 129–140. https://doi.org/10.1016/j.ympev.2018.04.007.
Kallal, R. J., & Hormiga, G. (2018). Systematics, phylogeny and biogeography of the Australasian leaf-curling orb-weaving spiders (Araneae: Araneidae: Zygiellinae), with comparative analysis of retreat evolution. Zoological Journal of the Linnean Society, 184, 1055–1141. https://doi.org/10.1093/zoolinnean/zly014.
Knoflach, B., & Van Harten, A. (2006). The one-palped spider genera Tidarren and Echinotheridion in the Old World (Araneae, Theridiidae), with comparative remarks on Tidarren from America. Journal of Natural History, 40, 1483–1616.
Kuntner, M., & Coddington, J. A. (2009). Discovery of the largest orbweaving spider species: The evolution of gigantism in Nephila. PLoS ONE, 4, e7516. https://doi.org/10.1371/journal.pone.0007516.
Kuntner, M., Hamilton, C. A., Cheng, R.-C., Gregorič, M., Lupše, N., Lokovšek, T., et al. (2019). Golden orbweavers ignore biological rules: phylogenomic and comparative analyses unravel a complex evolution of sexual size dimorphism. Systematic Biology, 68, 555–572. https://doi.org/10.1093/sysbio/syy082.
Legendre, P. (2018). Lmodel2: model II regression. R package version 1.7-3. https://CRAN.R-project.org/package=lmodel2.
LeGrand, R. S., & Morse, D. H. (2000). Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density. Biological Journal of the Linnean Society, 71, 643–664. https://doi.org/10.1006/bijl.2000.0466.
McLean, C. J., Garwood, R. J., & Brassey, C. A. (2018). Sexual dimorphism in the arachnid orders. PeerJ, 6, e5751. https://doi.org/10.7717/peerj.5751.
Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Evolutionary Biology, 36, 235–247.
Monteiro, L. R. (1999). Multivariate regression models and geometric morphometrics: The search for causal factors in the analysis of shape. Systematic Biology, 48, 192–199.
Montgomery, T. H. (1910). The significance of the courtship and secondary sexual characteristics of araneads. The American Naturalist, 44, 151–177.
Morbey, Y. E., & Ydenberg, R. C. (2008). Protandrous arrival timing to breeding areas: A review. Ecology Letters, 4, 663–673. https://doi.org/10.1046/j.1461-0248.2001.00265.x.
Moya-Laraño, J., Halaj, J., & Wise, D. H. (2002). Climbing to reach females: Romeo should be small. Evolution, 56, 420–425.
Moya-Laraño, J., Vinković, D., Allard, C., & Foellmer, M. W. (2007). Gravity still matters. Functional Ecology, 21, 1178–1181. https://doi.org/10.1111/j.1365-2435.2007.01335.x.
Moya-Laraño, J., & Foellmer, M. W. (2016). The gravity hypothesis. In T. K. Shackelford & V. A. Weekes-Shackelford (Eds.), Encyclopedia of evolutionary psychological science (pp. 1–7). Switzerland: Springer.
Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., Pearse, W. (2018). Caper: comparative analyses of phylogenetics and evolution. R package version 1.0.1. https://CRAN.R-project.org/package=caper.
Paradis, E., Blomberg, S., Bolker, B., Brown, J., Claude, J., Cuong, H.S. et al. (2018). Ape: Analyses of phylogenetics and evolution. R package version 5.2. https://CRAN.R-project.org/package=ape.
Prenter, J., Montgomery, W. I., & Elwood, R. W. (1995). Multivariate morphometrics and sexual dimorphism in the orb-web spider Metellina segmentata (Clerck, 1757) (Araneae, Metidae). Biological Journal of the Linnean Society, 55, 345–354.
Prenter, J., Perez-Staples, D., & Taylor, P. W. (2010). The effects of morphology and substrate diameter on climbing and locomotor performance in male spiders. Functional Ecology, 24, 400–408. https://doi.org/10.1111/j.1365-2435.2009.01633.x.
R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved August 1, 2019 from https://www.R-project.org/
Rensch, H. E. (1950). Die Abhängigkeit der relativen Sexualdifferenz von der Körpergrösse. Bonner Zoologische Beitrage, 1, 58–69.
Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 17–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x.
Rohlf, F.J. (2017). tpsDig2 Version 2.30 [Computer Software]. Stony Brook: Stony Brook University.
Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for optimal superimposition of landmarks. Systematic Zoology, 39, 40–59. https://doi.org/10.2307/2992207.
Sanger, T. J., Sherratt, E., McGlothlin, J. W., Brodie, E. D., III, Losos, J. B., & Abzhanov, A. (2013). Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution, 67, 2180–2193. https://doi.org/10.1111/evo.12100.
Santibáñez-López, C. E., Kriebel, R., & Sharma, P. P. (2017). Eadem figura manet: measuring morphological convergence in diplocentrid scorpions (Arachnida: Scorpiones: Diplocentridae) under a multilocus phylogenetic framework. Invertebrate Systematics, 31, 233–248. https://doi.org/10.1071/IS16078.
Scharff, N., & Coddington, J. A. (1997). A phylogenetic analysis of the orb-weaving spider family Araneidae (Arachnida, Araneae). Zoological Journal of the Linnean Society, 120, 355–434. https://doi.org/10.1111/j.1096-3642.1997.tb01281.x.
Scharff, N., Coddington, J.A., Blackledge, T.A., Agnarsson, I., Framenau, V.W., Szűts, T., et al. (2019). Phylogeny of the orb-weaving spider family Araneidae (Araneae: Araneoidea). Cladistics. https://doi.org/10.1111/cla.12382.
Schlager, S. (2017). Morpho and Rvcg—shape analysis in R. In G. Zheng, S. Li, & G. Szekely (Eds.), Statistical shape and deformation analysis (pp. 217–256). San Diego: Academic Press.
Shao, L., & Li, S. (2018). Early Cretaceous greenhouse pumped higher taxa diversification in spiders. Molecular Phylogenetics and Evolution, 127, 146–155. https://doi.org/10.1016/j.ympev.2018.05.026.
Sharma, P. P., Santiago, M. A., Kriebel, R., Lipps, S. M., Buenavente, P. A. C., Diesmos, A. C., et al. (2017). A multilocus phylogeny of Podoctidae (Arachnida, Opiliones, Laniatores) and parametric shape analysis reveal disutility of subfamilial nomenclature in armored harvestmen systematics. Molecular Phylogenetics and Evolution, 106, 163–173. https://doi.org/10.1016/j.ympev.2016.09.019.
Smith, H. M. (2006). A revision of the genus Poltys in Australasia (Araneae: Araneidae). Records of the Australian Museum, 58, 43–96.
Uhl, G., Schmidt, S., Martin, M. A., & Blanckenhorn, W. (2004). Food and sex-specific growth strategies in a spider. Evolutionary Ecology Research, 6, 523–540.
Uyeda, J. C., & Harmon, L. J. (2014). A novel Bayesian method for inferring and interpreting the dynamics of adaptive landscapes from phylogenetic comparative data. Systematic Biology, 63, 902–918. https://doi.org/10.1093/sysbio/syu057.
Uyeda, J. C., Pennell, M. W., Miller, E. T., Maia, R., & McClain, C. R. (2017). The evolution of energetic scaling across the vertebrate tree of life. The American Naturalist, 190, 185–199. https://doi.org/10.1086/692326.
Wheeler, W. C., Coddington, J. A., Crowley, L. M., Dimitrov, D., Goloboff, P. A., Griswold, C. E., et al. (2017). The spider tree of life: Phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics, 33, 574–616. https://doi.org/10.1111/cla.12182.
Webb, T. J., & Freckleton, R. P. (2007). Only half right: Species with female-biased sexual size dimorphism consistently break Rensch’s rule. PLoS ONE, 2, e897. https://doi.org/10.1371/journal.pone.0000897.
Wood, H. M., Gillespie, R. G., Griswold, C. E., & Wainwright, P. C. (2015). Why is Madagascar special? The extraordinarily slow evolution of pelican spiders (Araneae, Archaeidae). Evolution, 69, 462–481. https://doi.org/10.1111/evo.12578.
World Spider Catalog. (2019). World spider catalog, version 20.0. Natural History Museum Bern. Retrieved March 19, 2019 from http://wsc.nmbe.ch.
Yeargan, K. V. (1994). Biology of bolas spiders. Annual Review of Entomology, 39, 81–99.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. New York: Elsevier Academic Press.
Acknowledgements
We thank Matthias Foellmer and an anonymous reviewer for comments improving this manuscript. We thank Emma Sherratt, Mike Collyer, and Paul O’Higgins for their advice and guidance on data interpretation and analysis. We thank Thomas Guillerme for guidance using dispRity. We thank Hannah Wood and Tom Nguyen for loans from the Smithsonian Institution. We thank Joshua Storch, Josef Stiegler, and Alex Pyron for input in project ideation and analysis. This work was supported by US National Science Foundation grants DEB 1457300 and 1457539.
Funding
US National Science Foundation grants DEB 1457300 and 1457539 to Gustavo Hormiga and Gonzalo Giribet.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kallal, R.J., Moore, A.J. & Hormiga, G. The Shape of Weaver: Investigating Shape Disparity in Orb-Weaving Spiders (Araneae, Araneidae) Using Geometric Morphometrics. Evol Biol 46, 317–331 (2019). https://doi.org/10.1007/s11692-019-09482-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-019-09482-w