Sexual size dimorphism (SSD) is widespread among animals, but its developmental mechanisms are not fully undestood. We investigated the proximate causes of SSD in three male-larger and one monomorphic scarab beetles using detailed monitoring of growth in individual instars. Apart from the finding that SSD in all three male-larger species started to develop already in the first larval instar, we generally found a high variability in SSD formation among the species as well as among instars. Overall, sexual differences in developmental time, average growth rate, as well as in the shape of the growth trajectory seem to be the mechanisms responsible for SSD ontogeny in scarab beetles. In the third instar, when the larvae attain most of their mass, the males had a similar or even lower instantaneous growth rate than females and SSD largely developed as a consequence of a longer period of rapid growth in males even in cases when the sexes did not differ in the total duration of this instar. Our results demonstrate that a detailed approach, examining not only the average growth rate and developmental time, but also the shape of the growth trajectory, is necessary to elucidate the complex development of SSD.

Crop Research Institute Drnovská 507 16106 Praha 6 Ruzyně Czech Republic

Department of Ecology Faculty of Science Charles University Viničná 7 12844 Praha 2 Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 12844 Praha 2 Czech Republic

Zobrazit více v PubMed

Cox, R. M., Butler, M. A. & John-Alder, H. B. The evolution of sexual size dimorphism in reptiles in Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (ed. Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T.) 38–48 Oxford University Press (2007).

Kupfer, A. Sexual size dimorphism in amphibians: an overview in Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (ed. Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T.) 50–59 Oxford University Press (2007).

Abouheif E, Fairbairn DJ. A comparative analysis of allometry for sexual size dimorphism: Assessing Rensch’s rule. Am. Nat. 1997;149:540–562. doi: 10.1086/286004. DOI

Stillwell RC, Blanckenhorn WU, Teder T, Dawidowitz G, Fox CW. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu. Rev. Entomol. 2010;55:227–245. doi: 10.1146/annurev-ento-112408-085500. PubMed DOI PMC

Teder T. Sexual size dimorphism requires a corresponding sex diference in development time: a meta-analysis in insects. Funct. Ecol. 2014;28:479–486. doi: 10.1111/1365-2435.12172. DOI

Blanckenhorn WU, et al. Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am. Nat. 2007;169:245–57. PubMed

Tammaru T, Esperk T, Ivanov V, Teder T. Proximate sources of sexual size dimorphism in insects: locating constraints on larval growth schedules. Evol. Ecol. 2010;24:161–175. doi: 10.1007/s10682-009-9297-1. DOI

Stillwell RC, Davidowitz G. A developmental perspective on the evolution of sexual size dimorphism of a moth. Proc. R. Soc. Lond. B. 2010;277:2069–2074. doi: 10.1098/rspb.2009.2277. PubMed DOI PMC

Testa N, Ghosh SM, Shingleton AW. Sex specific weight loss mediates sexual size dimorphism in Drosophila melanogaster. PLoS One. 2013;8:e58936. doi: 10.1371/journal.pone.0058936. PubMed DOI PMC

Esperk T, Tammaru T, Nylin S, Teder T. Achieving high sexual size dimorphism in insects: females add instars. Ecol. Entomol. 2007;32:243–256. doi: 10.1111/j.1365-2311.2007.00872.x. DOI

Etilé E, Despland E. Developmental variation in the forest tent caterpillar: life history consequences of a threshold size for pupation. Oikos. 2008;117:135–143. doi: 10.1111/j.2007.0030-1299.16114.x. DOI

Christiansen P. Larval growth rates and sexual differences of resource allocation in the cetoniine scarab Mecynorhina polyphemus Fabricius 1781 (Coleoptera: Scarabaeidae: Goliathini) J. Nat. Hist. 2013;47:1287–1307. doi: 10.1080/00222933.2012.763061. DOI

Stillwell RC, Daws A, Davidowitz G. The ontogeny of sexual size dimorphism of a moth: when do males and females grow apart? PLoS One. 2014;9:e106548. doi: 10.1371/journal.pone.0106548. PubMed DOI PMC

Rohner PT, Blanckenhorn WU, Puniamoorthy N. Sexual selection on male size drives the evolution of male-biased sexual size dimorphism via the prolongation of male development. Evolution. 2016;70:1–11. doi: 10.1111/evo.12944. PubMed DOI

Wiklund C, Nylin S, Forsberg J. Sex-related variation in growth rate as a result of selection for large size and protandry in a bivoltine butterfly. Pieris napi. Oikos. 1991;60:241–250. doi: 10.2307/3544871. DOI

Gotthard K, Nylin S, Wiklund C. Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly. Pararge aegeria. Oecologia. 1994;99:281–289. doi: 10.1007/BF00627740. PubMed DOI

Knapp M. Emergence of sexual size dimorphism and stage-specific effects of elevated temperature on growth rate and development rate in Harmonia axyridis. Physiol. Entomol. 2014;39:341–347. doi: 10.1111/phen.12079. DOI

Nylin S, Wiklund C, Wickman P-O, Garcia-Barros E. Absence of trade-offs between sexual size dimorphism and early male emergence in a butterfly. Ecology. 1993;74:1414–1427. doi: 10.2307/1940071. DOI

Ernsting G, Isaaks JA. Gamete production and sexual size dimorphism in an insect (Orchesella cincta) with indeterminate growth. Ecol. Entomol. 2002;27:145–151. doi: 10.1046/j.1365-2311.2002.00395.x. DOI

Abbott JK, Svensson EI. Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly. J. Evol. Biol. 2005;18:1464–1470. doi: 10.1111/j.1420-9101.2005.01019.x. PubMed DOI

Abbott JK, Svensson EI. Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs. Evol. Ecol. 2008;22:103–121. doi: 10.1007/s10682-007-9161-0. DOI

Jarošík, V. & Honěk, A. Sexual differences in insect development time in relation to sexual size dimorphism in Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (ed. Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T.) 205–211 Oxford University Press (2007).

Molleman F, et al. Sexual differences in weight loss upon eclosion are related to life history strategy in Lepidoptera. J. Insect Physiol. 2011;57:712–722. doi: 10.1016/j.jinsphys.2011.02.009. PubMed DOI

Yasuda H, Dixon AFG. Sexual size dimorphism in the two spot ladybird beetle Adalia bipunctata: developmental mechanism and its consequences for mating. Ecol. Entomol. 2002;27:493–498. doi: 10.1046/j.1365-2311.2002.00428.x. DOI

Budrienė A, Budrys E, Nevronytė Ž. Sexual size dimorphism in the ontogeny of the solitary predatory wasp Symmorphus allobrogus (Hymenoptera: Vespidae) C. R. Biol. 2013;336:57–64. doi: 10.1016/j.crvi.2013.03.001. PubMed DOI

Nijhout HF. A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.) Biol. Bull. 1975;149:214–225. doi: 10.2307/1540491. PubMed DOI

Nijhout HF. Physiological control of molting in insects. Am. Zool. 1981;21:631–640. doi: 10.1093/icb/21.3.631. DOI

Tammaru T, Esperk T. Growth allometry of immature insects: larvae do not grow exponentially. Funct. Ecol. 2007;21:1099–1105. doi: 10.1111/j.1365-2435.2007.01319.x. DOI

Ayres MP, MacLean SF., Jr. Moult as a component of insect development, Gallerucella sagittariae (Chrysomelidae) and Epirrita autumnata (Geometridae) Oikos. 1987;48:273–279. doi: 10.2307/3565514. DOI

Vendl T, Kratochvíl L, Šípek P. Ontogeny of sexual size dimorphism in the hornless rose chafer Pachnoda marginata (Coleoptera: Scarabaeidae: Cetoniinae) Zoology. 2016;119:481–488. doi: 10.1016/j.zool.2016.07.002. PubMed DOI

Nijhout HF, Dawidowitz G, Roff DA. A quantitative analysis of the mechanism that controls body size in Manduca sexta. J. Biol. 2006;5:16. doi: 10.1186/jbiol43. PubMed DOI PMC

Rohner PT, Blanckenhorn WU, Schäfer MA. Critical weight mediates sexspecific body size plasticity and sexual dimorphism in the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae) Evol. Dev. 2017;19:147–156. doi: 10.1111/ede.12223. PubMed DOI

Reed DA, Beckage NE. Inhibition of testicular growth and development in Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata. J. Insect Physiol. 1997;43:29–38. doi: 10.1016/S0022-1910(96)00080-7. PubMed DOI

Ahrens D, Schwarzer J, Vogler AP. The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proc. R. Soc. B. 2014;281:20141470. doi: 10.1098/rspb.2014.1470. PubMed DOI PMC

Arrow, G. J. Horned beetles. A study of the fantastic in nature. The Hague: W. Junk Publishers (1951).

Eberhard WG. Beetle horn dimorphism: making the best of a bad lot. Am. Nat. 1982;119:420–426. doi: 10.1086/283920. DOI

Krikken J. A new key to the suprageneric taxa in the beetle family Cetoniidae, with annotated list of the known genera. Zool. Verhandel. 1984;210:1–77.

Šípek P, Král D. Immature stages of the rose chafers (Coleoptera: Scarabaeidae: Cetoniinae): a historical overview. Zootaxa. 2012;3323:1–16.

McMonigle, O. The complete guide to rearing flower and jewel scarabs. Elytra and Antenna (2006).

Klátil, L. & Vrána, T. Chov zlatohlávků a nosorožíků [Breeding of Flower and Rhinoceros beetles in captivity]. Robimaus – sdružení Magdaléna a Robert Javorských (2008). [In Czech].

Vendl T, Šípek P. Immature stages of giants: morphology and growth characteristics of Goliathus Lamarck, 1801 larvae indicate a predatory way of life (Coleoptera, Scarabaeidae, Cetoniinae) ZooKeys. 2016;619:25–44. doi: 10.3897/zookeys.619.8145. PubMed DOI PMC

Winsor CP. The Gompertz curve as a growth curve. Proc. Natl. Acad. Sci. USA. 1932;18:1–8. doi: 10.1073/pnas.18.1.1. PubMed DOI PMC

Folguera G, et al. An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. Comp. Biochem. Physiol. A. 2011;159:242–246. doi: 10.1016/j.cbpa.2011.03.002. PubMed DOI

Hernandez-Llamas A, Ratkowsky DA. Growth of fishes, crustaceans and molluscs: estimation of the Von Bertalanffy, Logistic, Gompertz and Richards curves and a new growth model. Mar. Ecol. Prog. Ser. 2004;282:237–244. doi: 10.3354/meps282237. DOI

von Bertalanffy L. Quantitative laws in metabolism and growth. Q. Rev. Biol. 1957;32:217–231. doi: 10.1086/401873. PubMed DOI

Lovich JE, Gibbons JW. A review of techniques for quantifying sexual size dimorphism. Growth Dev. Aging. 1992;56:269–281. PubMed

StatSoft I. STATISTICA, version 6.0. http://www.statsoft.com. (2001).

Callier V, Nijhout HF. Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc. Natl. Acad. Sci. USA. 2011;108:14664–14669. doi: 10.1073/pnas.1106556108. PubMed DOI PMC

Tanaka S, Mizue K. Studies on sharks – XV. Age and growth of Japanese dogfish, Mustelus manazo Bleeker in the East China Sea. Bull. Jpn. Soc. Sci. Fish. 1979;45:43–50. doi: 10.2331/suisan.45.43. DOI

Watkins GG. Proximate causes of sexual size dimorphism in the iguanian lizard Microlophus occipitalis. Ecology. 1996;77:1473–1482. doi: 10.2307/2265544. DOI

Frynta D, et al. Ontogeny of sexual size dimorphism in monitor lizards: Males grow for a longer period, but not at a faster rate. Zool. Sci. 2010;27:917–923. doi: 10.2108/zsj.27.917. PubMed DOI

Stamps J. Sexual size dimorphism in species with asymptotic growth after maturity. Biol. J. Linn. Soc. 1993;50:123–145. doi: 10.1111/j.1095-8312.1993.tb00921.x. DOI

Berrigan D, Charnov EL. Reaction norms for age and size at maturity in response to temperature: a puzzle for life historians. Oikos. 1994;70:474–478. doi: 10.2307/3545787. DOI

West GB, Brown JH, Enquist BJ. A general model for ontogenetic growth. Nature. 2001;413:628–631. doi: 10.1038/35098076. PubMed DOI

Ricklefs RE. Is rate of ontogenetic growth constrained by resource supply or tissue growth potential? A comment on West et al.’s model. Funct. Ecol. 2003;17:384–393. doi: 10.1046/j.1365-2435.2003.00745.x. DOI

Maino JL, Kearney MR. Testing mechanistic models of growth in insects. Proc. R. Soc. Lond. B. 2015;282:20151973. doi: 10.1098/rspb.2015.1973. PubMed DOI PMC

Kerkis J. The growth of the gonads in Drosophila melanogaster. Genetics. 1931;16:212–242. PubMed PMC

Wheeler DE, Tuchinskaya I, Buck NA, Tabashnik B. Hexameric storage proteins during metamorphosis and egg production in the diamondback moth, Plutella xylostella (Lepidoptera) J. Insect Physiol. 2000;46:951–958. doi: 10.1016/S0022-1910(99)00202-4. PubMed DOI

Telang A, Booton V, Chapman RF, Wheeler DE. How female caterpillars accumulate their nutrient reserves. J. Insect Physiol. 2001;47:1055–1064. doi: 10.1016/S0022-1910(01)00085-3. PubMed DOI

Milán M, Campuzano S, García-Bellido A. Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc. Natl. Acad. Sci. USA. 1996;93:640–645. doi: 10.1073/pnas.93.2.640. PubMed DOI PMC

Nijhout HF, Grunert LW. Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc. Natl. Acad. Sci. USA. 2002;99:15446–15450. doi: 10.1073/pnas.242548399. PubMed DOI PMC

Thermal Melanism in Pachnoda iskuulka (Coleoptera: Scarabaeidae: Cetoniinae)

Ontogeny of sexual size dimorphism revisited: Females grow for a longer time and also faster

First Case of Dual Size Asymmetry in an Identical Arthropod Organ: Different Asymmetries of the Combative (Sexual) and Cutting (Non-Sexual) Parts of Mandibles in the Horned Stored-Product Beetle Gnatocerus cornutus (Fabricius, 1798)