Abstract
Allometry is a common technique used by biologists to quantify and describe the exaggerated sexually selected traits of beetles. While horned species have dominated studies documenting weapon evolution among beetles, there is remarkable diversity in weapon type, including enormous mandibles, robust hind legs and elongated rostra. Here, I characterise intrasexual and intraspecific variation in body size, head size and shape in the anthribid weevil Hoherius meinertzhageni using traditional linear and 2D geometric morphometric approaches. Large males possess a broadened, shield-like head, which is much smaller in females and small-bodied males. Males were significantly larger in head and body size than females, and showed higher levels of variation in head and mandible size. Males exhibited an intrasexual dimorphism in head width and mandible length, but not head or antenna length. Overall, male head and mandible size showed hyperallometry, but minor males showed significantly steeper allometric slopes compared to major males and females. Geometric morphometrics revealed distinct differences in head shape between all groups (major and minor males, females). There were significant differences in the magnitude and direction of trajectories in size-shape space between males and females, with males showing more shape change per unit of size than females. In addition, there were significant differences in trajectory length but not slope angle between minor and major males. Overall, this combined approach using allometry with both traditional linear morphometrics and geometric morphometrics suggests that sexual selection is driving divergence in weapon size and shape among males and between the sexes. Preliminary behavioural observations support the hypothesis that weapon morphology corresponds to alternative mating tactics, although a more thorough investigation into the mating system of H. meinertzhageni is required.
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Code availability
R code used in all analyses will be made publicly available at the Open Science Framework after publication.
Data availability
Collection locality and measurement data are provided in Supplementary table 1. Shape data based on geometric morphometrics will be publicly available at the Open Science Framework after publication.
References
Adams DC, Collyer ML, Kaliontzopoulou A (2020a) Geomorph: software for geometric morphometric analyses. R Package Version 3(2):1
Adams DC, Glynne E, Kaliontzopoulou A (2020b) Interspecific allometry for sexual shape dimorphism: Macroevolution of multivariate sexual phenotypes with application to Rensch’s rule. Evolution 74:1908–1922. https://doi.org/10.1111/evo.14049
Bonduriansky R (2007) Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61:838–849. https://doi.org/10.1111/j.1558-5646.2007.00081.x
Bookstein F (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med Image Anal 1:225–243
Collyer ML, Adams DC (2018) RRPP: An r package for fitting linear models to high-dimensional data using residual randomization. Methods Ecol Evol 9:1772–1779. https://doi.org/10.1111/2041-210X.13029
Collyer ML, Adams DC (2020) RRPP: Linear Model Evaluation with Randomzied Residuals in a Permutation Procedure. https://cran.r-project.org/web/packages/RRPP
Cook JM, Bean D (2006) Cryptic male dimorphism and fighting in a fig wasp. Anim Behav 71:1095–1101
Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London
Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B Biol Sci 275:71–76
Eberhard WG, Gutierrez EE (1991) Male dimorphisms in beetles and earwigs and the question of developmental constraints. Evolution 45:18–28
Eberhard WG, Rodríguez RL, Huber BA et al (2018) Sexual selection and static allometry: the importance of function. Q Rev Biol 93:207–250
Emlen DJ (1997) Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41:335–341. https://doi.org/10.1007/s002650050393
Emlen DJ (2001) Costs and the diversification of exaggerated animal structures. Science 291:1534–1536. https://doi.org/10.1126/science.1056607
Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413. https://doi.org/10.1146/annurev.ecolsys.39.110707.173502
Emlen DJ, Marangelo J, Ball B, Cunningham CW (2005) Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060–1084
Gidaszewski NA, Baylac M, Klingenberg CP (2009) Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evol Biol 9:110. https://doi.org/10.1186/1471-2148-9-110
Glazier DS (2013) Log-transformation is useful for examining proportional relationships in allometric scaling. J Theor Biol 334:200–203. https://doi.org/10.1016/j.jtbi.2013.06.017
Goczał J, Rossa R, Tofilski A (2019) Intersexual and intrasexual patterns of horn size and shape variation in the European rhinoceros beetle: quantifying the shape of weapons. Biol J Linn Soc 127:34–43. https://doi.org/10.1093/biolinnean/blz026
Gotoh H, Cornette R, Koshikawa S et al (2011) Juvenile hormone regulates extreme mandible growth in male stag beetles. PLoS ONE 6:e21139. https://doi.org/10.1371/journal.pone.0021139
Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41:587–638. https://doi.org/10.1111/j.1469-185X.1966.tb01624.x
Holloway BA (1982) Fauna of New Zealand Number 3 Anthribidae (Insecta: Coleoptera). Science Information Division, DSIR, Wellington
Huxley JS (1932) Problems of relative growth. Methuen, London
Huxley JS, Teissier G (1936) Terminology of relative growth. Nature 137:780–781
Iguchi Y (2013) Male mandible trimorphism in the stag beetle Dorcus rectus (Coleoptera: Lucanidae). Eur J Entomol 110:159–163
Kelly CD (2005) Allometry and sexual selection of male weaponry in Wellington tree weta, Hemideina crassidens. Behav Ecol 16:145–152
Kelly C, Adams D (2010) Sexual Selection, Ontogenetic acceleration, and hypermorphosis generates male trimorphism in wellington tree weta. Evol Biol 37:200–209. https://doi.org/10.1007/s11692-010-9096-1
Kerkhoff AJ, Enquist BJ (2009) Multiplicative by nature: why logarithmic transformation is necessary in allometry. J Theor Biol 257:519–521. https://doi.org/10.1016/j.jtbi.2008.12.026
Kijimoto T, Pespeni M, Beckers O, Moczek AP (2013) Beetle horns and horned beetles: emerging models in developmental evolution and ecology. Wiley Interdiscip Rev Dev Biol 2:405–418. https://doi.org/10.1002/wdev.81
Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920. https://doi.org/10.1111/j.0014-3820.2002.tb00117.x
Knell RJ (2009) On the analysis of non-linear allometries. Ecol Entomol 34:1–11
Knell RJ, Pomfret JC, Tomkins JL (2004) The limits of elaboration: curved allometries reveal the constraints on mandible size in stag beetles. Proc R Soc B Biol Sci 271:523–528
Kodric-Brown A, Sibly RM, Brown JH (2006) The allometry of ornaments and weapons. PNAS 103:8733–8738. https://doi.org/10.1073/pnas.0602994103
LeGrice RJ, Tezanos-Pinto G, de Villemereuil P et al (2019) Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils. Evolution. https://doi.org/10.1111/evo.13698
Lenth RV (2016) Least-Squares Means: The R Package lsmeans. J Stat Softw 69: 1–33. https://doi.org/10.18637/jss.v069.i01
Lovich JE, Gibbons JW (1992) Review of techniques for quantifying sexual size dimorphism. Growth Dev Aging 56:269–281
Matsumoto K, Knell RJ (2017) Diverse and complex male polymorphisms in Odontolabis stag beetles (Coleoptera: Lucanidae). Sci Rep 7:16733
Matsuo Y (2005) Extreme eye projection in the male weevil exechesops leucopis (coleoptera: anthribidae): its effect on intrasexual behavioral interferences. J Insect Behav 18:465–477. https://doi.org/10.1007/s10905-005-5605-y
McCullough EL, Tobalske BW, Emlen DJ (2014) Structural adaptations to diverse fighting styles in sexually selected weapons. Proc Natl Acad Sci 111:14484–14488. https://doi.org/10.1073/pnas.1409585111
McCullough EL, Ledger KJ, Moore TY (2015) Variation in cross-sectional horn shape within and among rhinoceros beetle species. Biol J Linn Soc N/a-N/a. https://doi.org/10.1111/bij.12557
Moczek AP, Emlen DJ (2000) Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes? Anim Behav 59:459–466. https://doi.org/10.1006/anbe.1999.1342
Nijhout HF, Emlen DJ (1998) Competition among body parts in the development and evolution of insect morphology. Proc Natl Acad Sci U S A 95:3685–3689
O’Brien DM, Katsuki M, Emlen DJ (2017) Selection on an extreme weapon in the frog-legged leaf beetle (Sagra femorata). Evolution 71:2584–2598. https://doi.org/10.1111/evo.13336
Oliveira RF, Taborsky M, Brockmann HJ (2008) Alternative Reproductive Tactics - An Integrative Approach. Cambridge University Press, Cambridge
Packard GC (2009) On the use of logarithmic transformations in allometric analyses. J Theor Biol 257:515–518
Packard GC (2021) Is allometric variation in the cephalic horn on male rhinoceros beetles discontinuously dimorphic? Evol Biol 48:233–245
Painting CJ, Holwell GI (2013) Exaggerated trait allometry, compensation and trade-offs in the New Zealand giraffe Weevil (Lasiorhynchus barbicornis). PLoS ONE 8:e82467. https://doi.org/10.1371/journal.pone.0082467
Painting CJ, Holwell GI (2014a) Flexible alternative mating tactics by New Zealand giraffe weevils. Behav Ecol 25:1409–1416. https://doi.org/10.1093/beheco/aru140
Painting CJ, Holwell GI (2014b) Exaggerated rostra as weapons and the competitive assessment strategy of male giraffe weevils. Behav Ecol 25:1233–1239. https://doi.org/10.1093/beheco/aru119
Painting CJ, Buckley TR, Holwell GI (2014) Male-biased sexual size dimorphism and sex ratio in the New Zealand Giraffe Weevil, Lasiorhynchus barbicornis (Fabricius, 1775) (Coleoptera: Brentidae). Austral Entomol 53:317–327. https://doi.org/10.1111/aen.12080
Painting CJ, Probert AF, Townsend DJ, Holwell GI (2015) Multiple exaggerated weapon morphs: a novel form of male polymorphism in harvestmen. Sci Rep 5:16368. https://doi.org/10.1038/srep16368
Pélabon C, Tidière M, Lemaître J-F, Gaillard J-M (2018) Modelling allometry: statistical and biological considerations – a reply to Packard. Biol J Linn Soc 125:664–671. https://doi.org/10.1093/biolinnean/bly141
Pomfret JC, Knell RJ (2006) Sexual selection and horn allometry in the dung beetle Euoniticellus intermedius. Anim Behav 71:567–576
Powell S (2008) Ecological specialization and the evolution of a specialized caste in Cephalotes ants. Funct Ecol 22:902–911. https://doi.org/10.1111/j.1365-2435.2008.01436.x
Powell EC, Painting CJ, Hickey AJ, Holwell GI (2020) Defining an intrasexual male weapon polymorphism in a New Zealand harvestman (Opiliones: Neopilionidae) using traditional and geometric morphometrics. Biol J Linn Soc 130:395–409. https://doi.org/10.1093/biolinnean/blaa040
Prates MO, Cabral CRB, Lachos VH (2013) mixsmsn: fitting finite mixture of scale mixture of skew-normal distributions. J Stat Softw 54:1–20
R Core Development Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org:
Romiti F, Redolfi De Zan L, Piras P, Carpaneto GM (2016) Shape variation of mandible and head in Lucanus cervus (Coleoptera: Lucanidae): a comparison of morphometric approaches. Biol J Linn Soc 120:836–851. https://doi.org/10.1093/biolinnean/blw001
Rowland JM, Emlen DJ (2009) Two thresholds, three male forms result in facultative male trimorphism in beetles. Science 323:773–776. https://doi.org/10.1126/science.1167345
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Simmons LW, Emlen DJ (2006) Evolutionary trade-off between weapons and testes. Proc Natl Acad Sci U S A 103:16346–16351. https://doi.org/10.1073/pnas.0603474103
Tomkins JL, Kotiaho JS, LeBas NR (2005a) Matters of scale: Positive allometry and the evolution of male dimorphisms. Am Nat 165:389–402
Tomkins JL, Kotiaho JS, LeBas NR (2005b) Phenotypic plasticity in the developmental integration of morphological trade-offs and secondary sexual trait compensation. Proc R Soc B Biol Sci 272:543–551
Worthington AM, Berns CM, Swallow JG (2012) Size matters, but so does shape: quantifying complex shape changes in a sexually selected trait in stalk-eyed flies (Diptera: Diopsidae). Biol J Linn Soc 106:104–113. https://doi.org/10.1111/j.1095-8312.2011.01841.x
Yamane T, Okada K, Nakayama S, Miyatake T (2010) Dispersal and ejaculatory strategies associated with exaggeration of weapon in an armed beetle. Proc R Soc B Biol Sci 277:1705–1710. https://doi.org/10.1098/rspb.2009.2017
Yoshitake H, Kawashima I (2004) Sexual Dimorphism and Agonistic Behavior of Exechesops Leucopis (Jordan) (Coleoptera: Anthribidae: Anthribinae). Coleopt Bull 58:77–83. https://doi.org/10.1649/605
Zeh ZDW, JA, Tavakilian, G, (1992) Sexual Selection and Sexual Dimorphism in the Harlequin Beetle Acrocinus longimanus. Biotropica 24:86–96
Acknowledgements
Thank you to Oriane David for assistance with specimen landmarking, Pete McGregor for sharing locality and behaviour information and photographs of H. meinertzhageni, as well as sharing videos of the species behaviour, Greg Holwell for helpful comments on a draft of this manuscript, Emma Sherratt and Jaimi Gray for helpful geomorph advice, Grace Hall, Cor Vink and Phil Sirvid for assistance in the arthropod collections of New Zealand, Birgit Rhodes for assistance using the imaging microscope at Landcare Research, and Emma Scheltema for the illustrations. I thank Emma Sherratt for very helpful guidance as handling editor and two anonymous reviewers for their constructive suggestions. Finally, thank you to Robert Hoare for pointing out this fascinating beetle to me in the first place.
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I was supported by a Kate Edgar Educational Trust postdoctoral award during data collection, and a Rutherford Postdoctoral Fellowship during manuscript preparation.
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CJP conceived and designed the study, collected and analysed the data, and wrote the manuscript.
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Painting, C.J. Size and shape variation in the male dimorphic head weapons of an anthribid weevil (Hoherius meinertzhageni). Evol Ecol 36, 643–662 (2022). https://doi.org/10.1007/s10682-021-10127-8
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DOI: https://doi.org/10.1007/s10682-021-10127-8