, Volume 137, Issue 2, pp 291–304 | Cite as

Evolutionary negative allometry of orthopteran hind femur length is a general phenomenon

  • Claudio J. Bidau
  • Pablo A. Martínez
Original paper


1. Body size influences the way that organisms both perform their locomotor activities and perceive their environment. Allometry of insect legs with respect to body size is affected by many factors such as ontogenetic constraints and natural selection. Negative allometry, positive allometry, or isometry could result from different mechanisms influencing leg length and locomotion performance. 2. We tested three main models of hind femur length allometry (natural selection for jumping performance, ontogenetic constraint, and the size-grain model) in Orthoptera, a Polyneopteran order with large size range and high habitat and lifestyle diversification. We used a data set of 1549 species including members of both suborders, Ensifera and Caelifera, and many representative families using a Linear Mixed Model approach, and Reduced Major Axis and Ordinary Least Squares regression to explore evolutionary interspecific allometry in this order. 3. Our results showed a generalized trend of negative allometry (leg length decreases with body size increase) at the ordinal, subordinal, and familial levels, contrary to the expectations of the size-grain model and supporting our main hypothesis of a common ancestral developmental pattern regulating leg negative allometry in Orthoptera. 4. The conservation of a common hind leg allometric pattern in Orthoptera provides a basic framework to study adaptation of hind limbs to different habitats and lifestyles, and has important implications for the analysis of ecogeographic and evolutionary rules.


Jumping allometry Habitat coarseness Linear Mixed Model Ontogenetic allometry Sexual allometry Static allometry 



We are grateful to Andrea Cardini and an anonymous reviewer for their expert comments and suggestions that greatly improved the first version of the manuscript. We also wish to heartily thank Talita Ferreira Amado for graciously letting us to use her drawing of Dichroplus pratensis used for Fig. 1. CJB thanks Bettina Gordo D’Amico for her hospitality in Buenos Aires during the writing of this paper.

Compliance with ethical standards

This article complies with the journal’s ethical standards.

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animals rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

435_2018_395_MOESM1_ESM.docx (452 kb)
Appendix S1. The database of male and female body and femur 3 lengths of 1548 orthopteran species with the bibliographic references from which measurements was obtained. (DOCX 452 KB)
435_2018_395_MOESM2_ESM.docx (13 kb)
Appendix S2. Pairwise comparisons (male–male and female–female) of RMA regression slopes (log10femur3 length vs log10body length) between families of the orthopteran suborder Caelifera. Each cell shows the z-score and its statistical significance (ns= non-significant). Female–female results in bold type and italics. (DOCX 12 KB)
435_2018_395_MOESM3_ESM.docx (14 kb)
Appendix S3. Pairwise comparisons (male–male and female–female) of RMA regression slopes (log10femur3 length vs log10body length) between families of the orthopteran suborder Ensifera. Each cell shows the z-score and its statistical significance (ns= non-significant). Female–female results in bold type and italics. (DOCX 14 KB)


  1. Amédégnato C, Devriese H (2008) Global diversity of true and pygmy grasshoppers (Acridomorpha, Orthoptera) in freshwater. Hydrobiologia 595:535–543. CrossRefGoogle Scholar
  2. Angelini DR, Kaufman TC (2005) Insect appendages and comparative ontogenetics. Dev Biol 286:57–77. CrossRefPubMedGoogle Scholar
  3. Baena-Bejarano N (2015) Aspects of the natural history of Ripipteryx (Orthoptera: Rypipterygidae) species of Colombia. J Insect Behav 28:44–54. CrossRefGoogle Scholar
  4. Bailey WJ, Rentz DCF (1990) The Tettigoniidae, biology, systematics and evolution. Springer, Hong KongGoogle Scholar
  5. Barr TC Jr (1968) Cave ecology and the evolution of troglobites. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology. Springer, New York, pp 35–102CrossRefGoogle Scholar
  6. Bennet-Clark HC (1990) Jumping in Orthoptera. In: Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, pp 173–203Google Scholar
  7. Bidau CJ (2014) Patterns of Orthoptera biodiversity. I. Adaptations in ecological and evolutionary contexts. J Insect Biodivers 2(20):1–39. CrossRefGoogle Scholar
  8. Bidau CJ, Marti DA (2007) Clinal variation of body size in Dichroplus pratensis (Orthoptera: Acrididae): inversion of Bergmann’s and Rensch’s rules. Ann Entomol Soc Am 100:850–860. CrossRefGoogle Scholar
  9. Bidau CJ, Marti DA (2008a) Geographic and climatic factors related to a body size cline in Dichroplus pratensis Bruner, 1900 (Melanoplinae, Acrididae). J Orthoptera Res 17:140–156. CrossRefGoogle Scholar
  10. Bidau CJ, Marti DA (2008b) A test of Allen’s rule in ectotherms: the case of two South American Melanopline grasshoppers (Orthoptera: Acrididae) with partially overlapping geographic ranges. Neotrop Entomol 37:370–380. CrossRefPubMedGoogle Scholar
  11. Bidau CJ, Martí DA, Castillo ER (2013) Rensch’s rule is not verified in melanopline grasshoppers. J Insect Biodivers 1(12):1–14. CrossRefGoogle Scholar
  12. Bidau CJ, Taffarel A, Castillo ER (2016) Breaking the rule: multiple patterns of scaling of sexual size dimorphism with body size in orthopteroid insects. Rev Soc Entomol Argent 75:11–36Google Scholar
  13. Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174. CrossRefGoogle Scholar
  14. Bohonak AJ, van der Linde K (2004) RMA, software for reduced major axis regression. Java version.
  15. Boxshall GA (2004) The evolution of arthropod limbs. Biol Rev 79:253–300. CrossRefPubMedGoogle Scholar
  16. Bradshaw CJA, Brook WA (2010) The conservation biologist’s toolbox: principles for the design and analysis of conservation studies. In: Sodhi NS, Ehrlich PR (eds) Conservation biology for all. Oxford University Press, Oxford, pp 313–340CrossRefGoogle Scholar
  17. Bunnefeld N, Phillimore AB (2012) Island, archipelago and taxon effects: mixed models as a means of dealing with the imperfect design of nature's experiments. Ecography 35(1):15–22.
  18. Burns MD (1973) The control of walking in Orthoptera. J Exp Biol 58:45–58Google Scholar
  19. Burrows M, Picker MD (2010) Jumping mechanisms and performance of pygmy mole crickets (Orthoptera, Tridactylidae). J Exp Biol 213:2386–2398. CrossRefPubMedGoogle Scholar
  20. Burrows M, Sutton GP (2012) Pygmy mole crickets jump from water. Curr Biol 22: R990–R991. CrossRefPubMedGoogle Scholar
  21. Capinera JL (2008) Grasshoppers, katydids, and crickets (Orthoptera). In: Capinera JL (ed) Encyclopedia of entomology, 2nd edn. Springer, New York, pp 1694–1712CrossRefGoogle Scholar
  22. Chapman RF, Joern AR (1990) Biology of grasshoppers. Wiley, New YorkGoogle Scholar
  23. Chintauan-Marquier IC, Jordan S, Berthier P, Amédégnato C, Pompanon F (2011) Evolutionary history and taxonomy of a short-horned grasshopper subfamily: the Melanoplinae (Orthoptera: Acrididae). Mol Phylogenet Evol 58:22–32. CrossRefPubMedGoogle Scholar
  24. Chintauan-Marquier IC, Legendre F, Hugel S, Robillard T, Grandcolas P, Nel A, Zuccon D, Desutter-Grandcolas L (2016) Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis. Cladistics 32:54–81. CrossRefGoogle Scholar
  25. Clarke MRB (1980) The reduced major axis of a bivariate sample. Biometrika 67:441–446. CrossRefGoogle Scholar
  26. Culver DC (1982) Cave life-evolution and ecology. Harvard University Press, CambridgeCrossRefGoogle Scholar
  27. Delcomyn F (1981) Insect locomotion on land. In: Herreid CF II, Fourtner CR (eds) Locomotion and energetics in arthropods. Plenum, New York, pp 103–125CrossRefGoogle Scholar
  28. Eades DC, Otte D, Cigliano MM, Braun H (2017) Orthoptera species file. Version 5.0/5.0. Accesed December 2017
  29. Emlen DJ, Nijhout HF (2000) The development and evolution of exaggerated morphologies in insects. Annu Rev Entomol 45:661–708. CrossRefPubMedGoogle Scholar
  30. Espadaler X, Gómez C (2001) Formicine ants comply with the size-grain hypothesis. Funct Ecol 15:136–138. CrossRefGoogle Scholar
  31. Farji-Brener AG (2004) The size– grain hypothesis in ants: conflicting evidence or confounded perspective? Ecol Entomol 29:380–380. CrossRefGoogle Scholar
  32. Farji-Brener AG, Barrantes G, Ruggiero A (2004) Environmental rugosity, body size and access to food: a test of the size—grain hypothesis in tropical litter ants. Oikos 104:165–171. CrossRefGoogle Scholar
  33. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. CrossRefGoogle Scholar
  34. Fenn JD, Song H, Cameron SL, Whiting MF (2008) A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Mol Phylogenet Evol 49:59–68. CrossRefPubMedGoogle Scholar
  35. Field LH (2001) The biology of wetas and king crickets, and their allies. CABI, WallingfordCrossRefGoogle Scholar
  36. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of the evidence. Am Nat 160:712–726.$15.00CrossRefPubMedGoogle Scholar
  37. Gabriel JM (1985) The development of the locust jumping mechanism. I. Allometric growth and its effect on jumping performance. J Exp Biol 118:313–326Google Scholar
  38. Galecki A, Burzykowski T (2013) Linear mixed-effects models using R: a step-by-step approach. Springer, New YorkCrossRefGoogle Scholar
  39. Gaston KJ, Chown SL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500. CrossRefGoogle Scholar
  40. González-Megías A, Gómez JM, Sánchez-Piñero F (2007) Diversity-habitat heterogeneity relationship at different spatial and temporal scales. Ecography 30: 31–41. CrossRefGoogle Scholar
  41. Gordon MS, Blickhan R, Dabiri JO, Videler jj (2017) Animal locomotion: physical principles and adaptations. CRC Press, Boca RatonCrossRefGoogle Scholar
  42. Graham D (1978a) Unusual step patterns in the free walking grasshopper Neoconocephalus robustus: I. General features of the step patterns. J Exp Biol 73:147–157Google Scholar
  43. Graham D (1978b) Unusual step patterns in the free walking grasshopper Neoconocephalus robustus: II. A critical test of the leg interactions underlying different models of hexapod co-ordination. J Exp Biol 73:159–172Google Scholar
  44. Graham D (1985) Pattern and control of walking in insects. Adv Insect Physiol 18:31–140. CrossRefGoogle Scholar
  45. Günther KK (1992) Revision der familie Cylindrachetidae Giglio-Tos, 1914 (Orthoptera, Tridactyloidea). Deut Entomol Z NF 39:233–291. CrossRefGoogle Scholar
  46. Haley EL, Gray DA (2012) Mating behavior and dual-purpose armaments in a Camel Cricket. Ethology 118:49–56. CrossRefGoogle Scholar
  47. Hochkirch A, Gröning J (2008) Sexual size dimorphism in Orthoptera (sens. str.): a review. J Orthoptera Res 17:189–196. CrossRefGoogle Scholar
  48. Hoenen S, Marques MD (1998) Circadian patterns of migration of Strinatia brevipennis (Orthoptera: Phalangopsidae) inside a cave. Biol Rhythm Res 29:480–487. CrossRefGoogle Scholar
  49. Holt BJ, Jønsson KA (2014) Reconciling hierarchical taxonomy with molecular phylogenies. Syst Biol 63:1010–1017. CrossRefPubMedGoogle Scholar
  50. Houston TF (2007) Observations of the biology and immature stages of the sandgroper Cylindraustralia kochii (Saussure), with notes on some congeners (Orthoptera: Cylindrachetidae). Rec West Aust Mus 23:219–234CrossRefGoogle Scholar
  51. Imbrie J (1954) AmBiometrical methods in the study of invertebrate fossils. Bull Am Mus Nat Hist 108:211.252Google Scholar
  52. Ingrisch S, Rentz DCF (2009) Orthoptera (grasshoppers, locusts, katydids, crickets). In: Resh VH, Gardé RT (eds) Encyclopedia of insects, 2nd edn. Academic Press-Elsevier, Burlington, pp 732–743CrossRefGoogle Scholar
  53. Jost MC, Shaw KL (2006) Phylogeny of Ensifera (Hexapoda: Orthoptera) using three ribosomal loci, with implications for the evolution of acoustic communication. Mol Phylogenet Evol 38:510–530. CrossRefPubMedGoogle Scholar
  54. Kaspari M, Weiser MD (1999) The size-grain hypothesis and interspecific scaling in ants. Funct Ecol 13:530–538. CrossRefGoogle Scholar
  55. Kaspari M, Weiser MD (2007) The size-grain hypothesis: do macroarthropods see a fractal world? Ecol Entomol 32:279–282. CrossRefGoogle Scholar
  56. Katz SL, Gosline JM (1993) Ontogenetic scaling of jump performance in the African desert locust (Schistocerca gregaria). J Exp Biol 177:81–111Google Scholar
  57. Kelsh R, Weinzierl RO, White RA, Akam M (1994) Homeotic gene expression in the locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and abdominal-A proteins. Dev Genet 15:19–31. CrossRefPubMedGoogle Scholar
  58. Lavoie KH, Helf KL, Poulson TL (2007) The biology and ecology of North American cave crickets. J Cave Karst Stud 69:114–134Google Scholar
  59. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73: 1943–1967. CrossRefGoogle Scholar
  60. Levins R (1968) Evolution in changing environments: some theoretical explorations. Princeton University Press, PrincetonGoogle Scholar
  61. Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proc R Soc B 279: 1033–1040.
  62. Luiz OJ, Allen AP, Robertson DR, Floeter SR, Kulbicki M, Vigliola L, Becheler R, Madin JS (2013) Adult and larval traits as determinants of geographic range size among tropical reef fishes. Proc Natl Acad Sci 110: 16498–16502.
  63. Mahfooz N, Turchyn N, Mihajlovic M, Hrycaj S, Popadić A (2007) Ubx regulates differential enlargement and diversification of insect hind legs. PLoS One 2(9):e866. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Martinez PA, Marti DA, Molina WF, Bidau CJ (2013) Bergmann’s rule across the equator: a case study in Cerdocyon thous (Canidae). J Anim Ecol 82:997–1008. CrossRefPubMedGoogle Scholar
  65. Mayr E (1956) Geographical character gradients and climatic adaptation. Evolution 10:105–108. CrossRefGoogle Scholar
  66. McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52:845–854. CrossRefGoogle Scholar
  67. Mousseau TA (1997) Ectotherms follow the converse to Bergmann’s rule. Evolution 51:630–632. CrossRefPubMedGoogle Scholar
  68. Parr ZJE, Parr CL, Chown SL (2003) The size-grain hypothesis: a phylogenetic and field test. Ecol Entomol 28:475–481. CrossRefGoogle Scholar
  69. Partridge L, Coyne JA (1997) Bergmann’s rule in ectotherms: is it adaptive? Evolution 51:632–635. CrossRefPubMedGoogle Scholar
  70. Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  71. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131.
  72. Preston KA, Ackerly D-D (2004) The evolution of allometry in modular organisms. In: Pigliucci M, Preston K (eds) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, Oxford, pp 80–106Google Scholar
  73. Queathem E (1991) The ontogeny of grasshopper jumping performance. J Insect Physiol 37:129–138. CrossRefGoogle Scholar
  74. Rehn JA, Grant HJ Jr (1959) A review of the Romaleinae (Orthoptera; Acrididae) found in America north of Mexico. P Acad Nat Sci Phila 111:109–271Google Scholar
  75. Santer RD, Yamawaki Y, Rind FC, Simmons PJ (2005) Motor activity and trajectory control during escape jumping in the locust Locusta migratoria. J Comp Physiol A 191:965–975. CrossRefGoogle Scholar
  76. Schmidt-Nielsen K (1984) Scaling: why is animal size so important? Cambridge University Press, CambridgeCrossRefGoogle Scholar
  77. Schooley RL (2006) Spatial heterogeneity and characteristic scales of species-habitat relationships. Bioscience 56:533–537. CrossRefGoogle Scholar
  78. Scott j (2005) The locust jump: an integrated laboratory investigation. Adv Physiol Educ 29: 21–26. CrossRefPubMedGoogle Scholar
  79. Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen D (2007) Size and shape: the developmental regulation of static allometry in insects. BioEssays 29:536–548. CrossRefPubMedGoogle Scholar
  80. Shubin N, Tabin C, Carroll S (1997) Fossils, genes and the evolution of animal limbs. Nature 388:639–648. CrossRefPubMedGoogle Scholar
  81. Smith RJ (2009) Use and misuse of the reduced major axis for line-fitting. Am J Phys Anthropol 14:476–486. CrossRefGoogle Scholar
  82. Sobel EC (1990) The locust’s use of motion paralax to measure distance. J Comp Physiol A 167:579–588CrossRefPubMedGoogle Scholar
  83. Song H, Amédégnato C, Cigliano MM, Desutter-Grandcolas L, Heads SW, Huang Y, Otte D, Whitting MF (2015) 300 million years of diversification: elucidating the pattern of orthopteran evolution base don comprehensive taxón and gene sampling. Cladistics 31:621–651. CrossRefGoogle Scholar
  84. Stern DL, Emlen DJ (1999) The developmental basis for allometry in insects. Development 126:1091–1101PubMedGoogle Scholar
  85. Studier EH, Lavoie KH, Howarth FG (2002) Leg attenuation and seasonal femur length: mass relationships in cavernicolous crickets (Orthoptera: Gryllidae and Rhaphidophoridae). J Cave Karst Stud 64:126–131Google Scholar
  86. Sutton GP, Burrows M (2008) The mechanics of elevation control in locust jumping. J Comp Physiol A 194:557–563. CrossRefGoogle Scholar
  87. Teuscher M, Brändle M, Traxel V, Brandl R (2009) Allometry between leg and body length of insects: lack of support for the size–grain hypothesis. Ecol Entomol 34:718–724. CrossRefGoogle Scholar
  88. Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92. CrossRefGoogle Scholar
  89. Uvarov B (1966) Grasshoppers and locusts: a handbook of general acridology, vol I. Cambridge University Press, CambridgeGoogle Scholar
  90. Uvarov B (1977) Grasshoppers and locusts: a handbook of general acridology, vol II. Cambridge University Press, CambridgeGoogle Scholar
  91. Villani MG, Allee LL, Díaz A, Robbins PS (1999) Adaptive strategies of edaphic arthropods. Annu Rev Entomol 44:233–256. CrossRefPubMedGoogle Scholar
  92. Whitman DG (2008) The significance of body size in the Orthoptera, a review. J Orthoptera Res 17:117–134. CrossRefGoogle Scholar
  93. Wilson DM (1966) Insect walking. Annu Rev Entomol 11:103–122. CrossRefPubMedGoogle Scholar
  94. Zhang H, Shinmyo Y, Mito T, Miyawaki K, Sarashina I, Ohuchi H, Noji S (2005) Expression patterns of the homeotic genes Scr, Antp, Ubx, and abd-A during embryogenesis of the cricket Gryllus bimaculatus. Gene Expr Patterns 5:491–502. CrossRefPubMedGoogle Scholar
  95. Zhang Y, Huang H, Liu X, Ren L (2011) Kinematics of terrestrial locomotion in mole cricket Gryllotalpa orientalis. J Bionic Eng 8(2):151–157. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Olaguer 444Buenos AiresArgentina
  2. 2.Laboratorio de Pesquisas Integrativas em Biodiversidade (PIBi Lab)Universidade Federal de SergipeSão CristovãoBrazil

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