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Research articlesThree-dimensional geometric morphometric analysis of the skull of Protoceratops andrewsi supports a socio-sexual signalling role for the ceratopsian frill
Published:03 February 2021https://doi.org/10.1098/rspb.2020.2938
Abstract
Socio-sexual selection is predicted to be an important driver of evolution, influencing speciation, extinction and adaptation. The fossil record provides a means of testing these predictions, but detecting its signature from morphological data alone is difficult. There are, nonetheless, some specific patterns of growth and variation which are expected of traits under socio-sexual selection. The distinctive parietal-squamosal frill of ceratopsian dinosaurs has previously been suggested as a socio-sexual display trait, but evidence for this has been limited. Here, we perform a whole-skull shape analysis of an unprecedentedly large sample of specimens of Protoceratops andrewsi using a high-density landmark-based geometric morphometric approach to test four predictions regarding a potential socio-sexual signalling role for the frill. Three predictions—low integration with the rest of the skull, significantly higher rate of change in size and shape during ontogeny, and higher morphological variance than other skull regions—are supported. One prediction, sexual dimorphism in shape, is not supported, suggesting that sexual differences in P. andrewsi are likely to be small. Together, these findings are consistent with mutual mate choice or selection for signalling quality in more general social interactions, and support the hypothesis that the frill functioned as a socio-sexual signal in ceratopsian dinosaurs.
Footnotes
References
- 1.
Darwin C . 1871The descent of man and selection in relation to sex. London, UK: John Murray. Google Scholar - 2.
Ritchie MG . 2007Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38, 79-102. Crossref, ISI, Google Scholar - 3.
Maan ME, Seehausen O . 2011Ecology, sexual selection and speciation. Ecol. Lett. 14, 591-602. (doi:10.1111/j.1461-0248.2011.01606.x) Crossref, PubMed, ISI, Google Scholar - 4.
Janicke T, Ritchie MG, Morrow EH, Marie-Orleach L . 2018Sexual selection predicts species richness across the animal kingdom. Proc. R. Soc. B 285, 20180173. (Doi:10.1098/rspb.2018.0173) Link, ISI, Google Scholar - 5.
Martínez-Ruiz C, Knell RJ . 2016Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors. J. Anim. Ecol. 86, 117-127. (doi:10.1111/1365-2656.12601) Crossref, PubMed, ISI, Google Scholar - 6.
Cally JG, Stuart-Fox D, Holman L . 2019Meta-analytic evidence that sexual selection improves population fitness. Nat. Commun. 10, 2017. (doi:10.1038/s41467-019-10074-7) Crossref, PubMed, ISI, Google Scholar - 7.
Tobias JA, Montgomerie R, Lyon BE . 2012The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil. Trans. R. Soc. B 367, 2274-2293. (doi:10.1098/rstb.2011.0280) Link, ISI, Google Scholar - 8.
West-Eberhard MJ . 1979Sexual selection, social competition and evolution. Am. Philos. Soc. 123, 222-234. ISI, Google Scholar - 9.
West-Eberhard MJ . 1983Sexual selection, social competition and speciation. Q. Rev. Biol. 58, 155-183. (doi:10.1086/413215) Crossref, ISI, Google Scholar - 10.
Knell RJ, Naish D, Tompkins JL, Hone DWE . 2012Sexual selection in prehistoric animals: detection and implications. TREE 28, 38-47. Crossref, PubMed, ISI, Google Scholar - 11.
Padian K, Horner JR . 2010The evolution of ‘bizarre structures’ in dinosaurs: biomechanics, sexual selection, social selection or species recognition?J. Zool. 283, 3-17. (doi:10.1111/j.1469-7998.2010.00719.x) Crossref, ISI, Google Scholar - 12.
Knell RJ, Sampson S . 2011Bizarre structures in dinosaurs: species recognition or sexual selection? A response to Padian and Horner. J. Zool. 283, 18-22. (doi:10.1111/j.1469-7998.2010.00758.x) Crossref, ISI, Google Scholar - 13.
Hone DWE, Wood D, Knell RJ . 2016Positive allometry for exaggerated structures in the ceratopsian dinosaur Protoceratops andrewsi supports socio-sexual signalling. Palaeontol. Electron. 19.1.5A, 1-13. ISI, Google Scholar - 14.
Knapp A, Knell RJ, Farke AA, Loewen MA, Hone DWE . 2018Patterns of divergence in the morphology of ceratopsian dinosaurs: sympatry is not a driver of divergence. Proc. R. Soc. B 285, 20180312. (doi:10.1098/rspb.2018.0312) Link, ISI, Google Scholar - 15.
Hone DWE, Mallon JC . 2017Protracted growth impedes the detection of sexual dimorphism in non-avian dinosaurs. Palaeontology 60, 535-545. (doi:10.1111/pala.12298) Crossref, ISI, Google Scholar - 16.
Kokko H, Johnstone R . 2002Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 357, 319-330. (doi:10.1098/rstb.2001.0926) Link, ISI, Google Scholar - 17.
Kraaijeveld K, Kraaijeveld-Smit FJ, Komdeur J . 2007The evolution of mutual ornamentation. Anim. Behav. 74, 657-677. (doi:10.1016/j.anbehav.2006.12.027) Crossref, ISI, Google Scholar - 18.
Hooper PL, Miller G . 2008Mutual mate choice can drive costly signalling even under perfect monogamy. Adapt. Behav. 16, 53-69. (doi:10.1177/1059712307087283) Crossref, ISI, Google Scholar - 19.
O'Brien DM, Allen CE, Van Kleeck MJ, Hone DWE, Knell RJ, Knapp A, Christiansen S, Emlen DJ . 2018On the evolution of extreme structures: static scaling and the function of sexually selected signals. Anim. Behav. 144, 95-108. (doi:10.1016/j.anbehav.2018.08.005) Crossref, ISI, Google Scholar - 20.
Zelditch ML, Swiderski DL, Sheets HD, Fink WL . 2004Geometric morphometrics for biologists: a primer. London, UK: Elsevier. Google Scholar - 21.
Klingenberg CP . 2008Morphological integration and developmental modularity. Annu. Rev. Ecol. Syst. 39, 115-132. (doi:10.1146/annurev.ecolsys.37.091305.110054) Crossref, Google Scholar - 22.
Goswami A, Finarelli JA . 2016EMMLi: a maximum likelihood approach to the analysis of modularity. Evolution 70, 1622-1637. (doi:10.1111/evo.12956) Crossref, PubMed, ISI, Google Scholar - 23.
Felice RN, Watanabe A, Cuff AR, Noirault E, Pol D, Witmer LM, Norell MA, O'Connor PM, Goswami A . 2019Evolutionary integration and modularity in the archosaur cranium. Integr. Comp. Biol. 59, 371-382. (doi:10.1093/icb/icz052) Crossref, PubMed, ISI, Google Scholar - 24.
Felice RN, Randau M, Goswami A . 2018A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580-2594. (doi:10.1111/evo.13608) Crossref, PubMed, ISI, Google Scholar - 25.
Bardua C, Wilkinson M, Gower DJ, Sherratt E, Goswami A . 2019Morphological evolution and modularity of the caecilian skull. BMC Evol. Biol. 19, 30. (doi:10.1186/s12862-018-1342-7) Crossref, PubMed, ISI, Google Scholar - 26.
Watanabe A, Fabre AC, Felice RN, Maisano JA, Müller J, Herrel A, Goswami A . 2019Ecomorphological diversification in squamates from conserved pattern of cranial integration. Proc. Natl. Acad. Sci. USA 116, 14 688-14 697. (Doi:10.1073/pnas.1820967116) Crossref, ISI, Google Scholar - 27.
Bonduriansky R . 2007Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61, 838-849. (doi:10.1111/j.1558-5646.2007.00081.x) Crossref, PubMed, ISI, Google Scholar - 28.
Tomkins JL, LeBas NR, Witton MP, Martill DM, Humphries S . 2010Positive allometry and the prehistory of sexual selection. Am. Nat. 176, 141-148. (doi:10.1086/653001) Crossref, PubMed, ISI, Google Scholar - 29.
Prieto-Márquez A, Garcia-Porta J, Joshi SH, Norell MA, Makovicky PJ . 2020Modularity and heterochrony in the ceratopsian frill. Ecol. Evol. 10, 6268-6309. (doi:10.1002/ece3.6361) Crossref, ISI, Google Scholar - 30.
Evans KM, Bernt MJ, Kolmann MA, Ford KL, Albert JS . 2018Why the long face? Static allometry in the sexually dimorphic phenotypes of Neotropical electric fishes. Zool. J. Linn. Soc. 186, 633-649. (doi:10.1093/zoolinnean/zly076) Crossref, ISI, Google Scholar - 31.
Johnstone RA, Rands SA, Evans MR . 2009Sexual selection and condition-dependence. J. Evol. Biol. 22, 2387-2394. (doi:10.1111/j.1420-9101.2009.01822.x) Crossref, PubMed, ISI, Google Scholar - 32.
Kammerer CF, Deutsch M, Lungmus JK, Angielczyk KD . 2020Effects of taphonomic deformation on geometric morphometric analysis on fossils: a study using the dicynodont Diictodon feliceps (Therapsida, Anomodontia). PeerJ. 8, e9925. (doi:10.7717/peerj.9925) Crossref, PubMed, ISI, Google Scholar - 33.
Dodson P . 1976Quantitative aspects of relative growth and sexual dimorphism in Protoceratops. J. Paleontol. 50, 929-940. ISI, Google Scholar - 34.
Maiorino L, Farke AA, Kotsakis T, Piras P . 2015Males resemble females: re-evaluating sexual dimorphism in Protoceratops andrewsi (Neoceratopsia, Protoceratopsidae). PLoS ONE 10, e0126464. (doi:10.1371/journal.pone.0126464) Crossref, PubMed, ISI, Google Scholar - 35.
Goswami A, Watanabe A, Felice RN, Bardua C, Fabre AC, Polly PD . 2019High-density morphometric analysis of shape and integration: the good, the bad, and the not-really-a-problem. Integr. Comp. Biol. 59, 669-683. (doi:10.1093/icb/icz120) Crossref, PubMed, ISI, Google Scholar - 36. AgiSoft PhotoScan Professional (Version 1.4.3) (Software). 2019Retrieved from: http://www.agisoft.com/downloads/installer/. Google Scholar
- 37.
- 38.
Lautenschlager S . 2016Reconstructing the past: methods and techniques for the digital restoration of fossils. R. Soc. Open Sci. 3, 160342. (doi:10.1098/rsos.160342) Link, ISI, Google Scholar - 39.
Bardua C, Felice RN, Watanabe A, Fabre AC, Goswami A . 2019A practical guide to sliding and surface semilandmarks in morphometric analyses. Integr. Organism. Biol. 1, Obz016. (doi:10.1093/iob/obz016) Crossref, Google Scholar - 40. R Core Team. 2013R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www.R-project.org/. Google Scholar
- 41.
Schlager S . 2017Morpho and Rvcg—shape analysis in R. In Statistical shape and deformation analysis (edsZheng G, Li S, Szekely G ). London, UK: Academic Press. Google Scholar - 42.
Cardini A . 2016Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. J. Zool. Syst. Evol. Res. 55, 1-10. (doi:10.1111/jzs.12144) Crossref, ISI, Google Scholar - 43.
Adams DC, Otárola-Castillo E . 2013Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393-399. (doi:10.1111/2041-210X.12035) Crossref, ISI, Google Scholar - 44.
Angielczyk KD, Sheets HD . 2007Investigation of simulated tectonic deformation in fossils using geometric morphometrics. Paleobiology 33, 125-148. (doi:10.1666/06007.1) Crossref, ISI, Google Scholar - 45.
Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL . 2004Comparison of cranial ontogenetic trajectories among great apes and humans. J. Hum. Evol. 46, 679-698. (doi:10.1016/j.jhevol.2004.03.006) Crossref, PubMed, ISI, Google Scholar - 46.
Goswami A, Polly PD . 2010Methods for studying morphological integration and modularity. In Quantitative methods in paleobiology (edsAlroy J, Hunt G ), pp. 213-243. Cambridge, UK: Paleontological Society. Google Scholar - 47.
Maechler M . 2016diptest: Hartigan's dip test statistic for unimodality—corrected. R package version 0.75-7. See https://CRAN.R-project.org/package=diptest. Google Scholar - 48.
Dodson P, Forster CA, Sampson SD . 2004Ceratopsidae. In The Dinosauria (edsWeishampel DB, Dodson P, Osmólska H ). Berkeley, CA: University of California Press. Google Scholar - 49.
Czepiński Ł . 2019Ontogeny and variation of a protoceratopsid dinosaur Bagaceratops rozhdestvenskyi from the Late Cretaceous of the Gobi Desert. Hist. Biol. 32, 1394-1421. (doi:10.1080/08912963.2019.1593404) Crossref, ISI, Google Scholar - 50.
Snively E, Cox A . 2008Structural mechanics of pachycephalosaur crania permitted head-butting behavior. Palaeontol. Electron. 11, 3A:17p. ISI, Google Scholar - 51.
Cooney CR, MacGregor HEA, Seddon N, Tobias JA . 2018Multi-modal signal evolution in birds: re-examining a standard proxy for sexual selection. Proc. R. Soc. B 285, 20181557. (doi:10.1098/rspb.2018.1557) Link, ISI, Google Scholar - 52.
Hedrick BP, Dodson P . 2013Lujiatun Psittacosaurids: understanding individual and taphonomic variation using 3D geometric morphometrics. PLoS ONE 8, e69265. (doi:10.1371/journal.pone.0069265) Crossref, PubMed, ISI, Google Scholar - 53.
Mallon JC . 2017Recognizing sexual dimorphism in the fossil record: lessons from nonavian dinosaurs. Paleobiology 43, 495-507. (doi:10.1017/pab.2016.51) Crossref, ISI, Google Scholar - 54.
Moorhouse RJ . 1996The extraordinary bill dimorphism of the Huia (Heteraclocha acutirostris): sexual selection or intersexual competition?Notornis 43, 19-34. Google Scholar - 55.
Butler M 2007Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447, 202-205. (doi:10.1038/nature05774) Crossref, PubMed, ISI, Google Scholar - 56.
Felice RN, O'Connor PM . 2016The evolution of sexually dimorphic tail feathers is not associated with tail skeleton dimorphism. J. Avian Biol. 47, 371-377. (doi:10.1111/jav.00801) Crossref, ISI, Google Scholar - 57.
Funghi C, Trigo S, Gomes ACR, Soares MC, Cardoso GC . 2018Release from ecological constraint erases sex differences in social ornamentation. Behav. Ecol. Sociobiol. 72, 67. (doi:10.1007/s00265-018-2486-6) Crossref, ISI, Google Scholar - 58.
Shuker DM . 2009Sexual selection: endless forms or tangled bank?Anim. Behav. 79, 11-17. (doi:10.1016/j.anbehav.2009.10.031) Crossref, ISI, Google Scholar
