Skip to main content

Advertisement

Log in

Did Adult Diurnal Activity Influence the Evolution of Wing Morphology in Opoptera Butterflies?

  • Systematics, Morphology and Physiology
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The butterfly genus Opoptera includes eight species, three of which have diurnal habits while the others are crepuscular (the usual activity period for members of the tribe Brassolini). Although never measured in the field, it is presumed that diurnal Opoptera species potentially spend more time flying than their crepuscular relatives. If a shift to diurnal habits potentially leads to a higher level of activity and energy expenditure during flight, then selection should operate on increased aerodynamic and energetic efficiency, leading to changes in wing shape. Accordingly, we ask whether diurnal habits have influenced the evolution of wing morphology in Opoptera. Using phylogenetically independent contrasts and Wilcoxon rank sum tests, we confirmed our expectation that the wings of diurnal species have higher aspect ratios (ARs) and lower wing centroids (WCs) than crepuscular congeners. These wing shape characteristics are known to promote energy efficiency during flight. Three Opoptera wing morphotypes established a priori significantly differed in AR and WC values. The crepuscular, cloud forest dweller Opoptera staudingeri (Godman & Salvin) was exceptional in having an extended forewing tip and the highest AR and lowest WC within Opoptera, possibly to facilitate flight in a cooler environment. Our study is the first to investigate how butterfly wing morphology might evolve as a response to a behavioral shift in adult time of activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig 1
Fig 2
Fig 3

Similar content being viewed by others

References

  • Barber JR, Leavell BC, Keener AL, Breinholt JW, Chadwell BA, McClure CJW, Hill G, Kawahara AY (2015) Moth tails divert bat attack: evolution of acoustic deflection. Proc Natl Acad Sci Biol. doi:10.1073/pnas.1421926112

    Google Scholar 

  • Berwaerts K, Van Dyck H, Aerts P (2002) Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct Ecol 16:484–491

    Article  Google Scholar 

  • Berwaerts K, Matthysen E, Van Dyke H (2008) Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment. Evolution 62:2525–2533

    Article  PubMed  Google Scholar 

  • Betts CR, Wootton RJ (1988) Wing shape and fight behavior in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. J Exp Biol 138:271–288

    Google Scholar 

  • Casagrande MM, Mielke OH (2000) Larva de quinto estádio e pupa de Dasyophthalma rusina rusina (Godart) (Lepidoptera, Nymphalidae, Brassolinae). Rev Bras Zool 17:401–404

    Article  Google Scholar 

  • Cespedes A, Penz CM, DeVries PJ (2015) Cruising the rain forest floor: butterfly wing shape evolution and gliding in ground effect. J Anim Ecol. doi:10.1111/1365-2656.12325

    PubMed  Google Scholar 

  • Chai P, Dudley R (1996) Limits to flight energetics of hummingbirds hovering in hypodense and hypoxic gas mixtures. J Exp Biol 199:2285–2295

    PubMed  CAS  Google Scholar 

  • Chai P, Srygley RB (1990) Predation and the flight, morphology, and temperature of neotropical rain-forest butterflies. Am Nat 135:748–765

    Article  Google Scholar 

  • DeVries PJ (1987) Butterflies of Costa Rica and their natural history, Vol. 1: Papilionidae, Pieridae, Nymphalidae. Princeton University Press, Princeton

    Google Scholar 

  • DeVries PJ, Penz CM, Hill RI (2010) Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol 79:1077–1085

    Article  PubMed  CAS  Google Scholar 

  • Dockx C (2007) Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.), in Cuba. Biol J Linn Soc 92:605–616

    Article  Google Scholar 

  • Dudley R (2000) The biomechanics of insect flight: form, function, evolution. Princeton University Press, Princeton

    Google Scholar 

  • Ellington CP (1984) The aerodynamics of hovering insect flight. II. Morphological parameters. Philos Trans R Soc B 305:17–40

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Freitas AVL, Benson WW, Marini-Filho OJ, De Carvalho RM (1997) Territoriality by the dawn’s early light: the Neotropical owl butterfly Caligo idomenaeus (Nymphalidae: Brassolinae). J Res Lep 34:14–20

    Google Scholar 

  • Fruhstorfer H (1912) Family: Brassolidae. In: Seitz A (ed) Die Gross-Schmetterlinge der Erde, Vol. 5. Alfred Kernen, Stuttgart, pp 285–332

    Google Scholar 

  • Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Article  Google Scholar 

  • Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Article  Google Scholar 

  • Grafen A (1989) The phylogenetic regression. Philos Trans R Soc B 326:119–157

    Article  CAS  Google Scholar 

  • Hill JK, Thomas CD, Blakeley DS (1999) Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia 121:165–170

    Article  Google Scholar 

  • Jantzen B, Eisner T (2008) Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera. Proc Natl Acad Sci Biol 105:16636–16640

    Article  Google Scholar 

  • Kingsolver JG (1999) Experimental analyses of wing size, flight, and survival in the western white butterfly. Evolution 53:1479–1490

    Article  Google Scholar 

  • Kingsolver JG, Srygley RB (2000) Experimental analysis of body size, flight and survival in pierid butterflies. Evol Ecol Res 2:593–612

    Google Scholar 

  • Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.71

  • Marden JH (1987) Maximum lift production during takeoff in flying animals. J Exp Biol 130:235–258

    Google Scholar 

  • Marden JH, Chai P (1991) Aerial predation and butterfly design: how palatability, mimicry, and the need for evasive flight constrain mass allocation. Am Nat 138:15–36

    Article  Google Scholar 

  • Outomuro D, Adams DC, Johansson F (2013a) Wing shape allometry and aerodynamics in calopterygid damselflies: a comparative approach. BMC Evol Biol 13:1–11

    Article  Google Scholar 

  • Outomuro D, Adams DC, Johansson F (2013b) The evolution of wing shape in ornamented-winged damselflies (Calopterygidae, Odonata). Evol Biol 40:300–309

    Article  Google Scholar 

  • Outomuro D, Cordero-Rivera A, Nava‐Bolaños A, Córdoba‐Aguilar A (2014) Does allometry of a sexually selected ornamental trait vary with sexual selection intensity? A multi‐species test in damselflies. Ecol Entomol 39:399–403

    Article  Google Scholar 

  • Park H, Bae K, Lee B, Jeon WP, Choi H (2010) Aerodynamic performance of a gliding swallowtail butterfly wing model. Exp Mech 50:1313–1321

    Article  Google Scholar 

  • Penz CM (2007) Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Syst Entomol 32:668–689

    Article  Google Scholar 

  • Penz CM (2009) The phylogeny of Opoptera butterflies, and an assessment of the systematic position of O. staudingeri (Lepidoptera, Nymphalidae). Zootaxa 1985:1–20

    Google Scholar 

  • Penz CM, Freitas AVL, Kaminski LA, Casagrande MM, DeVries PJ (2013) Adult and early-stage characters of Brassolini contain conflicting phylogenetic signal (Lepidoptera, Nymphalidae). Syst Entomol 38:316–333

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Robbins RK (1981) The “false head” hypothesis: predation and wing pattern variation of lycaenid butterflies. Am Nat 116:770–775

    Article  Google Scholar 

  • Rohlf FJ, Chang WS, Sokal RR, Kim J (1990) Accuracy of estimated phylogenies: effects of tree topology and evolutionary model. Evolution 44:1671–1684

    Article  Google Scholar 

  • Rutowski RL (1991) The evolution of mate-locating behavior in butterflies. Am Nat 138:1121–1139

    Article  Google Scholar 

  • Srygley RB (1994) Shivering and its cost during reproductive behavior in Neotropical owl butterflies, Caligo and Opsiphanes (Nymphalidae: Brassolinae). Anim Behav 47:23–32

    Article  Google Scholar 

  • Srygley RB (2001) Sexual differences in tailwind drift compensation in Phoebis sennae butterflies (Lepidoptera: Pieridae) migrating over seas. Behav Ecol 12:607–611

    Article  Google Scholar 

  • Srygley RB, Chai P (1990) Flight morphology of Neotropical butterflies: palatability and distribution of mass to the thorax and abdomen. Oecologia 84:491–499

    Article  Google Scholar 

  • Srygley RB, Penz CM (1999) The lek mating system in Neotropical owl butterflies: Caligo illioneus and C. oileus (Lepidoptera Brassolinae). J Insect Behav 12:81–103

    Article  Google Scholar 

  • Stone GN, Amos JN, Stone TF, Knight RL, Gay H, Parrott F (1988) Thermal effects on activity patterns and behavioural switching in a concourse of foragers on Stachytarpheta mutabilis (Verbenaceae) in Papua New Guinea. Oecologia 77:56–73

    Article  Google Scholar 

  • Uehara-Prado M, Freitas AVL, Francini RB, Brown KS Jr (2004) Guia das borboletas frugívoras da reserva estadual do Morro Grande e região de Caucaia do Alto, Cotia (São Paulo). Biota Neotrop 4:1–25

    Article  Google Scholar 

  • Wickman P-O (1992) Sexual selection and butterfly design—a comparative study. Evolution 46:1525–1536

    Article  Google Scholar 

  • Wootton RJ, Evans KE, Herbert R, Smith CW (2000) The hind wing of the desert locust (Schistocerca gregaria Forskal). I. Functional morphology and mode of operation. J Exp Biol 203:2921–2931

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

For access to specimens used in this study, we thank curators of the American Museum of Natural History, USA; Instituto de Biodiversidad, Costa Rica; Los Angeles County Museum, USA; McGuire Center for Lepidoptera and Biodiversity, University of Florida, USA; and Milwaukee Public Museum. Thanks also go to Isidro Chacón for providing specimen images and Phil DeVries for comments on a previous draft of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C M Penz.

Additional information

Edited by André VL Freitas – UNICAMP

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Penz, C.M., Heine, K.B. Did Adult Diurnal Activity Influence the Evolution of Wing Morphology in Opoptera Butterflies?. Neotrop Entomol 45, 50–57 (2016). https://doi.org/10.1007/s13744-015-0338-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-015-0338-x

Keywords

Navigation