Abstract
While the phenomenon of male mate choice has attracted considerable attention in the last two decades, whether this sexual selection mechanism could drive the evolution of female ornaments remains poorly understood. Here, we used experimental manipulation of female wing coloration to investigate male mate choice in Pieris rapae, a gift-giving butterfly. Further, we tested whether males’ nutritional status influenced their mating preferences by subjecting larvae to short periods of starvation. We found that males showed significantly more mating approaches toward control females with more colorful wings (higher pteridine content), and that this preference was strongest in low-nutrition males. Additionally, a study of field-collected females revealed that pteridine-based wing coloration was positively correlated with female egg load, which suggests such ornaments may signal female quality. Pteridine-based ornaments are widespread in nature, however their potential as honest signals in male mate choice remains largely unexplored. This work furthers our understanding of how male mate choice and female ornamentation may evolve in species whose mating systems include nutritional nuptial gifts.
Similar content being viewed by others
References
Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155
Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci U S A 6:13155–13160
Andersson J, Borg-Karlson A, Wiklund C (2003) Antiaphrodisicas in Pierid butterflies: a theme with variation! J Chem Ecol 29:1489–1499
Arikawa K, Wakakuwa M, Qiu X, Kurasawa M, Stavenga DG (2005) Sexual dimorphism of short-wavelength photoreceptors in the small white butterfly, Pieris rapae crucivora. J Neurosci 25:5935–5942
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Ann Rev Entomol 47:817–844
Boggs CL (1981) Nutritional and life-history determinants of resource allocation in holometabolous insects. Am Nat 117:692–709
Boggs CL (1995) Male nuptial gifts: Phenotypic consequences and evolutionary implications. In: Leather SR, Hardie J (eds) Insect reproduction. CRC, Boca Raton, pp 215–242
Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev Camb Philos Soc 76:305–339
Bonduriansky R (2009) Reappraising sexual coevolution and the sex-roles. PLoS Biol 7:e1000255
Burley N (1977) Parental investment, mate choice, and mate quality. Proc Natl Acad Sci U S A 74:3476–3479
Byrne PG, Rice WR (2006) Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc R Soc Lond B 273:917–922
Chenoweth SF, Doughty P, Kokko H (2006) Can non-directional male preferences facilitate honest female ornamentation? Ecol Lett 9:179–184
Chenoweth SF, Petfield D, Doughty P, Blows MW (2007) Male choice generates stabilizing sexual selection on a female fecundity correlate. J Evol Biol 20:1745–1750
Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77:3–11
Cornwallis CK, Birkhead TR (2007) Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity. Proc R Soc B 274:583–590
Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765
Darwin C (1874) The descent of man and selection in relation to sex, 2nd edn. American Home Library, New York
Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654
Eguchi E, Watanabe K, Hariyama T, Yamammoto K (1982) A comparison of electrophysiologically determined spectral responses in 35 species of Lepidoptera. J Insect Physiol 28:675–682
Ellers J, Boggs CL (2003) The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies. Evolution 57:1100–1106
Fitzpatrick S, Berglund A, Rosenqvist G (1995) Ornaments or offspring–costs to reproductive success restrict sexual selection processes. Biol J Linn Soc 55:251–260
Foote CJ, Brown GS, Hawryshyn CW (2004) Female colour and male choice in sockeye salmon: implications for the phenotypic convergence of anadromous and nonanadromous morphs. Anim Behav 67:69–83
Forero MG, Tella JL, Donazar JA, Blanco G, Bertellotti M, Ceballos O (2001) Phenotypic assortative mating and within-pair sexual dimorphism and its influence on breeding success and offspring quality in Magellanic penguins. Can J Zool 79:1414–1422
Frankino WA (2009) Experimental approaches to studying the evolution of morphological allometries: The shape of things to come. Invited submission in: Experimental Evolution: Concepts, Methods, and Applications. T. Garland, M. Rose (eds), University of California Press
Frankino WA, Zwaan BJ, Stern DL, Brakefield PM (2007) Internal and external constraints in the evolution of a forewing-hindwing allometry. Evolution 61:2958–2970
Giraldo MA, Stavenga DG (2007) Sexual dichroism and pigment localization in the wing scales of Pieris rapae butterflies. Proc R Soc B 247:97–102
Hardling R, Kokko H (2005) The evolution of prudent choice. Evol Ecol Res 7:697–715
Heisohn R, Legge S, Endler JA (2005) Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619
Holveck M-J, Geberzahn N, Riebel K (2011) An experimental test of condition-dependent male and female mate choice in zebra finches. PLoS ONE 6:e23974
Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391
Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931–2940
Kayser H (1985) In: Kerkut GA, Gilbert LI (eds) Pigments. Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, New York, pp 367–415
Kemp DJ (2007) Female butterflies prefer males bearing bright iridescent ornamentation. Proc R Soc B 274:1043–1047
Kemp DJ, Macedonia JM (2007) Male mating bias and its potential reproductive consequence in the butterfly Colias eurytheme. Behav Ecol Sociobiol 61:415–422
Knüttel H, Fiedler K (2001) Host-plant-derived variation in ultraviolet wing patterns influences mate selection by male butterflies. J Exp Biol 204:2447–2459
Kokko H (1998) Should advertising parental care be honest? Proc R Soc Lond B 265:1871–1878
Kokko H, Johnstone RA (2002) Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc 357:319–330
Kokko H, Monaghan P (2001) Predicting the direction of sexual selection. Ecol Lett 4:159–165
Kraaijeveld K, Gregurke J, Hall C, Komdeur J, Mulder RA (2004) Mutual ornamentation, sexual selection, and social dominance in the black swan. Behav Ecol 15:380–389
Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J (2007) The evolution of mutual ornamentation. Anim Behav 62:1021–1026
Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
LeBas NR, Hockham LR, Ritchie MG (2003) Nonlinear and correlational sexual selection on ‘honest’ female ornamentation. Proc R Soc Lond B 270:2159–2164
Lee T (2007) Female ornamentation and intrasexual competition in the convict cichlid fish (Archocentrus nigrofasciatus). PhD thesis, UCLA
Lewis SM, South A (2012) Evolution of animal nuptial gifts. Adv Study Behav 44:53–97
Lewis S, South A, Al-Wathiqui N, Burns R (2011) Quick guide: nuptial gifts. Curr Biol 21:644–645
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221
Morales J, Velando A, Torres R (2009) Fecundity compromises attractiveness when pigments are scarce. Behav Ecol 20:117–123
Morehouse NI (2009) Sexually selected male color ornament advertises direct and indirect benefits in a butterfly. Limiting nutrients, female choice, and male color. PhD thesis, Arizona State University
Morehouse NI, Rutowski RL (2010) In the eyes of the beholders: Female choice and avian predation risk associated with an exaggerated male butterfly color. Am Nat 176:768–784
Morehouse NI, Vukusic P, Rutowski R (2007) Pteridine pigment granules are responsible for both broadband light scattering and wavelength selective absorption in the wing scales of pierid butterflies. Proc R Soc Lond B 274:359–366
Nandy B, Joshi A, Ali ZS, Sen S, Prasad NG (2012) Degree of adaptive male mate choice is positively correlated with female quality variance. Sci Rep 2:447
Nordeide JT, Kekäläinen J, Janhunen M, Kortet R (2013) Female ornaments revisited—are they correlated with offspring quality? J Anim Ecol 82:26–38
Obara Y (1970) Studies on the mating behavior of the white cabbage butterfly, Pieris rapae crucivora Boisduval III. Near-ultra-violet. Z Vergl Physiol 69:99–116
Obara Y, Hidaka T (1968) Recognition of the female by the male, on the basis of ultra-violet reflection, in the white cabbage butterfly, Pieris rapae crucivora Boisduval. Proc Jpn Acad 44:829–832
Obara Y, Majerus MEN (2000) Initial mate recognition in the British cabbage butterfly, Pieris rapae rapae. Zool Sci 17:725–730
Obara Y, Ozawa G, Fukano Y, Watanabe K, Satoh T (2008) Mate preference in males of the cabbage butterfly, Pieris rapae crucivora, changes seasonally with the change in female UV color. Zool Sci 25:1–5
Obika M, Bagnara JT (1964) Pteridines as pigments in amphibians. Science 143:485–487
Owens IPF, Thompson DBA (1994) Sex differences, sex ratios and sex roles. Proc R Soc B 258:93–99
Parker GA (1983) Mate quality and mating decisions. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 141–164
Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K (2005) Male mate choice influences female promiscuity in Soay sheep. Proc R Soc B 272:365–373
Real L (1990) Search theory and mate choice. I. Models of single-sex discrimination. Am Nat 136:376–404
Rivero A, Giron D, Casas J (2001) Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect. Proc R Soc Lond B 268:1231–1237
Rutowski RL (1980) Courtship solicitation by females of the Checkered White butterfly, Pieris protodice. Behav Ecol Sociobiol 7:113–117
Rutowski RL (1981) Sexual discrimination using visual cues in the checkered white butterfly (Pieris protodice). Z Tierpsychol 55:325–334
Rutowski RL, Macedonia JM, Morehouse N, Taylor-Taft L (2005) Pteridine wing pigmentation amplify iridescent ultraviolet signal in males of the orange sulphur butterfly, Colias eurytheme. Proc R Soc B 272:2329–2335
Sæther SA, Fiske P, Kålås JA (2001) Male mate choice, sexual conflict and strategic allocation of copulations in a lekking bird. Proc R Soc B 268:2097–2102
Scriber JM, Slansky F Jr (1981) Nutritional ecology of immature insects. Annu Rev Entomol 26:183–211
Servedio MR (2007) Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement. Evolution 61:2772–2789
Setchell JM, Wickings EJ (2002) Mate choice in male mandrills (Mandrillus sphinx). Ethology 12:91–99
Shapiro JP, Ferkovich SM (2002) Yolk protein immunoassays (YP-ELISA) to assess diet and reproductive quality of mass-reared Orius insidiosus (Heteroptera: Anthocoridae). J Econ Entomol 95:927–935
Silberglied RE (1984) Visual communication and sexual selection among butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic, London, pp 207–223
Silberglied RE, Taylor OR (1978) Ultraviolet reflection and its behavioral role in the courtship of the sulphur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behav Ecol Sociobiol 3:203–243
Simmons LW, Emlen DJ (2008) No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius. J Evol Biol 21:1227–1235
Slansky F Jr, Rodriguez JG (1987) Nutritional ecology of insects, mites, spiders and related invertebrates: an overview. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, London, pp 1–69
South A, Lewis SM (2011) The influence of male ejaculate quantity on female fitness: a meta-analysis. Biol Rev 86:299–309
Stavenga DG, Stowe S, Siebke K, Zeil J, Arikawa K (2004) Butterfly wing colours: scale beads make white pierid wings brighter. Proc R Soc B 271:1577–1584
Steffen JE, McGraw KJ (2007) Contributions of pteridine and carotenoid pigments to dewlap coloration in two anole species. Comp Biochem Physiol B 146:42–46
Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol A 130:191–199
Suzuki Y (1979) Mating frequency in females of the small cabbage white, Pieris rapae crucivora Boisduval (Lepidoptera: Pieridae). Kontyu 47:335–339
Suzuki Y, Nakanishi A, Shima H, Yata O, Saigusa T (1977) Mating behavior in four Japanese species of the genus Pieris (Lepidoptera, Pieridae). Kontyu 45:300–313
Thomas DB, McGoverin CM, McGraw KJ, James HF, Madden O (2013) Vibrational spectroscopic analyses of unique yellow feather pigments (spheniscins) in penguins. J R Soc Interface 10
Tigreros N (2013) Linking nutrition and sexual selection across life stages in a model butterfly system. Funct Ecol 27:145–154
Tigreros N, Sass EM, Lewis SM (2013) Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly. Evol Ecol 27:1145–1158
Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos Trans R Soc B 367:2274–2293
Tudor MS, Morris MR (2009) Variation in male mate preference for female size in the swordtail Xiphophorus malinche. Behaviour 146:727–740
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142
Wall R, Wearmouth VJ, Smith KE (2002) Reproductive allocation by the blow fly Lucilia sericata in response to protein limitation. Physiol Entomol 27:267–274
Watt WB, Chew FS, Snyder LRG, Watt AG, Rothschild DE (1977) Population structure of pierid butterflies. I. Numbers and movements of some montane Colias species. Oecologia 27:1–22
Wedell N, Karlsson B (2003) Paternal investment directly affects female reproductive effort in an insect. Proc R Soc Lond B 270:2065–2071
Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizards (Sceloporus virgatus). Behav Ecol 17:726–732
Weiss SL, Foersterc K, Hudond J (2012) Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus). Comp Biochem Physiol B Biochem Mol Biol 161:117–123
Weiss SL, Kennedy EA, Safran RJ, McGraw KJ (2011) Pterin-based ornamental coloration predicts yolk antioxidant levels in female striped plateau lizards (Sceloporus virgatus). J Anim Ecol 80:519–527
Wheeler J, Dt G, Bussière LF (2012) Stabilizing sexual selection for female ornaments in a dance fly. J Evol Biol 25:1233–1242
Wijnen B, Leertouwer HL, Stavenga DG (2007) Colors and pterin pigmentation of pierid butterfly wings. J Insect Physiol 53:1206–1217
Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53:205–214
Acknowledgments
We thank Francie Chew for many helpful discussions throughout this project, and Durwood Marshall for statistical advice. This research was supported by an NSF REU award, and Sigma Xi and Tufts Graduate School Research awards to N.T.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. Kemp
Rights and permissions
About this article
Cite this article
Tigreros, N., Mowery, M.A. & Lewis, S.M. Male mate choice favors more colorful females in the gift-giving cabbage butterfly. Behav Ecol Sociobiol 68, 1539–1547 (2014). https://doi.org/10.1007/s00265-014-1764-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-014-1764-1