Evolutionary Ecology

, Volume 33, Issue 1, pp 71–87 | Cite as

Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila

  • Julián PadróEmail author
  • Juan Vrdoljak
  • Pablo Milla Carmona
  • Ignacio M. Soto
Original Paper


The rapid diversification of sexual traits is a common phenomenon accompanying the evolution of reproductive isolation, yet the evolutionary mechanisms driving such diversification are often unknown. Based on experimentally evolved strains of two sister species of cactophilic Drosophila, we investigated the correlated evolution of primary and secondary sexual traits to semi-natural environments enriched in secondary metabolites. We compared patterns of morphological evolution in the size and shape of male wing and genitalia of Drosophila buzzatii and Drosophila koepferae selected for different levels of alkaloid intensities for 20 generations. We found similar modes of selection operating among organs but not among species. The evolution of these traits in D. koepferae were compatible with patterns of stabilizing selection, while in D. buzzatii were characterized by directional changes. We also found that allometric variation was an important component of genital shape evolution, whereas changes in the wing morphology were less pronounced and mostly non-allometric. Overall, our data suggest that the diversification of sexual traits in this species pair is related to the evolution of dissimilar genetic architectures and reinforced by divergent ecological responses.


Alkaloid Chemical stress Experimental evolution Genitalia Morphological evolution Wing 



We thank B. Colines, D. De Panis and three anonymous reviewers whose comments greatly helped to improve the manuscript. This work was supported by the National Research Council of Argentina (CONICET) and Funded by the National Agency for Scientific and Technological Promotion (PICT 2017-0220), CONICET (PIP 112,201,500,100,423 CO) and University of Buenos Aires (UBACyT Mod I 2018-2019).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10682_2018_9964_MOESM1_ESM.docx (144 kb)
Supplementary material 1 (DOCX 143 kb)


  1. Arnqvist G (1997) The evolution of animal genitalia: distinguishing between hypotheses by single species studies. Biol J Linn Soc 60:365–379Google Scholar
  2. Arnqvist G, Thornhill R (1998) Evolution of animal genitalia: patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in water strider (Heteroptera: Gerridae: Insecta). Genet Res 71(3):193–212Google Scholar
  3. Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc R Soc Lond B Biol Sci 272(1566):877–886Google Scholar
  4. Barker JSF, Starmer WT (eds) (1982) Ecological genetics and evolution: the cactus-yeast-Drosophila model system. Academic Press, CambridgeGoogle Scholar
  5. Blows MW, Brooks R, Kraft PG (2003) Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies. Evolution 57(7):1622–1630Google Scholar
  6. Bonhomme V, Picq S, Gaucherel C, Claude J (2014) Momocs: outline analysis using R. J Stat Softw 56:1–24Google Scholar
  7. Brazner JC, Etges WJ (1993) Pre-mating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. II. Effects of larval substrates on time to copulation, mate choice and mating propensity. Evol Ecol 7(6):605–624Google Scholar
  8. Brodie ED, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10(8):313–318Google Scholar
  9. Carreira VP, Soto IM, Mensch J, Fanara JJ (2011) Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Dev Biol 11(1):32Google Scholar
  10. Chippindale AK, Chu TJ, Rose MR (1996) Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50(2):753–766Google Scholar
  11. Chippindale AK, Gibbs AG, Sheik M, Yee KJ, Djawdan M, Bradley TJ, Rose MR (1998) Resource acquisition and the evolution of stress resistance in Drosophila melanogaster. Evolution 52(5):1342–1352Google Scholar
  12. Colines B, Soto IM, de Panis DN, Padró J (2018) Experimental hybridization in allopatric species of the Drosophila repleta group (Diptera: Drosophilidae): implications for the mode of speciation. Biol J Linn Soc 123(2):290–301Google Scholar
  13. Coyne JA (1993) The genetics of an isolating mechanism between two sibling species of Drosophila. Evolution 47:778–788Google Scholar
  14. De Panis DN, Padró J, Furió-Tarí P, Tarazona S, Milla Carmona PS, Soto IM, Dopazo H, Conesa A, Hasson E (2016) Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Mol Ecol 25(18):4534–4550Google Scholar
  15. Debat V, Bégin M, Legout H, David JR (2003) Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature. Evolution 57(12):2773–2784Google Scholar
  16. Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, LondonGoogle Scholar
  17. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18(4):586–608Google Scholar
  18. Etges WJ (1992) Premating isolation is determined by larval substrates in cactophilic Drosophila mojavensis. Evolution 46:1945–1950Google Scholar
  19. Etges WJ, Tripodi AD (2008) Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. VIII. Mating success mediated by epicuticular hydrocarbons within and between isolated populations. J Evol Biol 21(6):1641–1652Google Scholar
  20. Fanara JJ, Soto IM, Lipko P, Hasson E (2016) First record of Drosophila buzzatii (Patterson & Wheeler)(Diptera: Drosophilidae) emerging from a non-cactus host. Neotrop Entomol 45(3):333–335Google Scholar
  21. Franco FF, Manfrin MH (2013) Recent demographic history of cactophilic Drosophila species can be related to quaternary palaeoclimatic changes in South America. J Biogeogr 40(1):142–154Google Scholar
  22. Gidaszewski NA, Baylac M, Klingenberg CP (2009) Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evol Biol 9(1):110Google Scholar
  23. Gilchrist AS, Partridge L (1999) A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153(4):1775–1787Google Scholar
  24. Gilchrist AS, Partridge L (2001) The contrasting genetic architecture of wing size and shape in Drosophila melanogaster. Heredity 86(2):144–152Google Scholar
  25. Harshman LG, Hoffmann AA, Clark AG (1999) Selection for starvation resistance in Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses. J Evol Biol 12(2):370–379Google Scholar
  26. Heinen-Kay JL, Noel HG, Layman CA, Langerhans RB (2014) Human-caused habitat fragmentation can drive rapid divergence of male genitalia. Evol Appl 7(10):1252–1267Google Scholar
  27. Hoffmann AA, Hercus MJ (2000) Environmental stress as an evolutionary force. Bioscience 50(3):217–226Google Scholar
  28. Hoikkala A, Aspi J (1993) Criteria of female mate choice in Drosophila littoralis, D. montana, and D. ezoana. Evolution 47(3):768–777Google Scholar
  29. House CM, Lewis Z, Hodgson DJ, Wedell N, Sharma MD, Hunt J, Hosken DJ (2013) Sexual and natural selection both influence male genital evolution. PLoS ONE 8(5):e63807Google Scholar
  30. Hurtado J, Soto EM, Orellana L, Hasson E (2012) Mating success depends on rearing substrate in cactophilic Drosophila. Evol Ecol 26:733–743Google Scholar
  31. Hurtado J, Iglesias PP, Lipko P, Hasson E (2013) Multiple paternity and sperm competition in the sibling species Drosophila buzzatii and Drosophila koepferae. Mol Ecol 22(19):5016–5026Google Scholar
  32. Iglesias PP, Soto EM, Soto IM, Colines B, Hasson E (2018) The influence of developmental environment on courtship song in cactophilic Drosophila. J Evol Biol. Google Scholar
  33. Iwata H, Ukai Y (2002) SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic fourier descriptors. J Hered 93:384–385Google Scholar
  34. Jagadeeshan S, Singh RS (2006) A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of male genitalia. J Evol Biol 19:1058–1070Google Scholar
  35. Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Res 11(2):353–357Google Scholar
  36. Klingenberg CP, Marugán-Lobón J (2013) Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. Syst Biol 62(4):591–610Google Scholar
  37. Krebs RA, Barker JSF (1993) Coexistence of ecologically similar colonising species. II. Population differentiation in Drosophila aldrichi and D. buzzatii for competitive effects and responses at different temperatures and allozyme variation in D. aldrichi. J Evol Biol 6(2):281–298Google Scholar
  38. Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comput Gr Image Process 18:236–258Google Scholar
  39. Langerhans RB, Anderson CM, Heinen-Kay JL (2016) Causes and consequences of genital evolution. Integr Comp Biol 56(4):741–751Google Scholar
  40. Lorch PD, Proulx S, Rowe L, Day T (2003) Condition-dependent sexual selection can accelerate adaptation. Evol Ecol Res 5(6):867–881Google Scholar
  41. Manfrin MH, Sene FM (2006) Cactophilic Drosophila in South America: a model for evolutionary studies. Genetica 126:57–75Google Scholar
  42. Manfrin MH, De Brito ROA, Sene FM (2001) Systematics and evolution of the Drosophila buzzatii (Diptera: Drosophilidae) cluster using mtDNA. Ann Entomol Soc Am 94(3):333–346Google Scholar
  43. Mardia KV, Bookstein FL, Moreton IJ (2000) Statistical assessment of bilateral symmetry of shapes. Biometrika 2:285–300Google Scholar
  44. Markow TA, O’Grady PM (2005) Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots. Annu Rev Genet 39:263–291Google Scholar
  45. Menezes BF, Vigoder FM, Peixoto AA, Varaldi J, Bitner-Mathé BC (2013) The influence of male wing shape on mating success in Drosophila melanogaster. Anim Behav 85(6):1217–1223Google Scholar
  46. Meyer JM, Fogleman JC (1987) Significance of saguaro cactus alkaloids in ecology of Drosophila mettleri, a soil-breeding, cactophilic drosophilid. J Chem Ecol 13(11):2069–2081Google Scholar
  47. Ogunbodede O, McCombs D, Trout K, Daley P, Terry M (2010) New mescaline concentrations from 14 taxa/cultivars of Echinopsis spp. (Cactaceae) (“San Pedro”) and their relevance to shamanic practice. J Ethnopharmacol 131(2):356–362Google Scholar
  48. Padró J, Carreira V, Corio C, Hasson E, Soto IM (2014) Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii. J Evol Biol 27(12):2781–2797Google Scholar
  49. Padró J, De Panis DN, Vrdoljak J, Carmona PM, Colines B, Hasson E, Soto IM (2018) Experimental evolution of alkaloid tolerance in sibling Drosophila species with different degrees of specialization. Evol Biol 45(2):170–181. Google Scholar
  50. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371Google Scholar
  51. Parsons PA (1994) Morphological stasis: an energetic and ecological perspective incorporating stress. J Theor Biol 171(4):409–414Google Scholar
  52. Partridge L, Ewing A, Chandler A (1987) Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim Behav 35(2):555–562Google Scholar
  53. Piccinali R, Aguadé M, Hasson E (2004) Comparative molecular population genetics of the Xdh locus in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Mol Biol Evol 21(1):141–152Google Scholar
  54. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Reinhardt K (2010) Natural selection and genital variation: a role for the environment, parasites and sperm ageing? Genetica 138(1):119–127Google Scholar
  56. Reti L, Castrillón JA (1951) Cactus alkaloids. I. Trichocereus terscheckii (Parmentier) Britton and Rose. J Am Chem Soc 73:1767–1769Google Scholar
  57. Richmond MP (2014) The role of aedeagus size and shape in failed mating interactions among recently diverged taxa in the Drosophila mojavensis species cluster. BMC Evol Biol 14(1):255Google Scholar
  58. Richmond MP, Johnson S, Markow TA (2012) Evolution of reproductive morphology among recently diverged taxa in the Drosophila mojavensis species cluster. Ecol Evol 2(2):397–408Google Scholar
  59. Roff DA (2000) Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence. J Evol Biol 13(3):434–445Google Scholar
  60. Rohlf FJ (2015) The tps series of software. Hystrix 26(1):9–12Google Scholar
  61. Rosenthal GA, Berenbaum MR (2012) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes, vol 2. Academic Press, LondonGoogle Scholar
  62. Santos M, Ruiz A, Barbadilla A, Quezada-Díaz JE, Hasson E, Fontdevila A (1988) The evolutionary history of Drosophila buzzatii. XlV. Larger flies mate more often in nature. Heredity 61:255–262Google Scholar
  63. Sgro CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93(3):241Google Scholar
  64. Simmons LW, House CM, Hunt J, García-González F (2009) Evolutionary response to sexual selection in male genital morphology. Curr Biol 19(17):1442–1446Google Scholar
  65. Soto IM (2012) Aedeagal divergence in sympatric populations of two sibling species of cactophilic Drosophila (Diptera: Drosophilidae): evidence of character displacement? Neotrop Entomol 41(3):207–213Google Scholar
  66. Soto IM, Carreira VP, Fanara JJ, Hasson E (2007) Evolution of male genitalia: environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids. BMC Evol Biol 7:1Google Scholar
  67. Soto IM, Carreira VP, Soto EM, Hasson E (2008) Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila. J Evol Biol 21(2):598–609Google Scholar
  68. Soto IM, Carreira VP, Soto EM, Márquez F, Lipko P, Hasson E (2013) Rapid divergent evolution of male genitalia among populations of Drosophila buzzatii. Evol Biol 40:395–407Google Scholar
  69. Soto IM, Carreira VP, Corio C, Padró J, Soto EM, Hasson E (2014) Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii. PLoS ONE 9(2):e88370Google Scholar
  70. StatSoft Inc. (2001) Statistica User’s Guide. Release 6.0 Edition, StatSoft Inc., Tulsa, OKGoogle Scholar
  71. Stefanini MI, Carmona PM, Iglesias PP, Soto EM, Soto IM (2018) Differential rates of male genital evolution in sibling species of Drosophila. Evol Biol 45:211–222. Google Scholar
  72. Trotta V, Cavicchi S, Guerra D, Andersen DH, Babbitt GA, Kristensen TN, Pedersen KS, Loeschcke V, Pertoldi C (2011) Allometric and non-allometric consequences of inbreeding on Drosophila melanogaster wings. Biol J Linn Soc 102(3):626–634Google Scholar
  73. Van Doorn GS, Edelaar P, Weissing FJ (2009) On the origin of species by natural and sexual selection. Science 326:1704–1707Google Scholar
  74. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53(1):205–214Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA – CONICET), DEGE, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  2. 2.Ecotono Laboratory, INIBIOMA, CONICETUniversidad Nacional del ComahueBarilocheArgentina
  3. 3.Instituto Patagónico para el Estudio de los Ecosistemas Continentales, Consejo Nacional de Investigaciones Científicas y Técnicas (IPEEC-CONICET)Puerto MadrynArgentina
  4. 4.Laboratorio de Ecosistemas Marinos FósilesInstituto de Estudios Andinos Don Pablo Groeber (CONICET-UBA)Buenos AiresArgentina

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