Abstract
In Beijing, China, females of Harmonia axyridis are promiscuous but prefer typical (succinea form) males to melanic ones in the spring generation, ostensibly due to the thermal disadvantages of melanism during summer. We used laboratory observations to test whether males invested differentially in females according to their elytral color, and whether male behavior was phenotype-dependent. Video-recording was used to monitor no-choice mating tests between virgin adults in all phenotype combinations and females were isolated post-copula to observe their egg retention times and reproduction over 5 days. Females tended to wait longer before using the sperm of melanic males, and melanic females delayed longer than succinic females. Melanic males spent longer in copula with succinic than melanic females and the latter received fewer bouts of male abdominal shaking that correlate with sperm transfer, regardless of the phenotype of their mate. Although melanic males abandoned melanic females faster than did succinic males, they remained in copula with females of both phenotypes for a longer period after shaking, suggesting a larger investment in mate guarding by the less-preferred male phenotype. Although female fecundity did not vary among phenotype combinations, egg fertility was lower for females mated to melanic males, suggesting a pleiotropic effect of melanism on male fertility in addition to its effects on male mating behavior.
Similar content being viewed by others
References
Alexander RD, Marshall DC, Cooley JR (1997) Evolutionary perspectives on insect mating. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 4–31
Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Ann Rev Entomol 56:21–40
Benham BR, Lonsdale D, Muggleton J (1974) Is polymorphism in two-spot ladybird an example of non-industrial melanism? Nature 249:179–180
Bonduransky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339
Brakefield PM (1984a) Ecological studies on the polymorphic ladybird Adalia bipunctata in the Netherlands. I. Population biology and geographical variation of melanism. J Anim Ecol 53:761–774
Brakefield PM (1984b) Ecological studies on the polymorphic ladybird Adalia bipunctata in the Netherlands. II. Population dynamics, differential timing of reproduction and thermal melanism. J Anim Ecol 53:775–790
Brakefield PM, Wilmer PG (1985) The basis of thermal melanism in the ladybird Adalia bipunctata. Differences in reflectance and thermal properties between morphs. Heredity 54:9–14
Clusella Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245
Creed ER (1966) Geographic variation in the two-spot ladybird in England and Wales. Heredity 21:57–72
Davies L, Bouvet S, Vernon P (2007) All-year reproduction and possible thermal melanism in Amblystogenium pacificum (Coleoptera: Carabidae) on the sub-Antarctic Ile de la Possession (Iles Crozet). Polar Biol 30:253–260
de Jong PW, Verhoog MD, Brakefield PM (1993) Sperm competition and melanic polymorphism in the 2-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae). Heredity 70:172–178
de Jong PW, Brakefield PM, Geerinck BP (1998) The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Behav Ecol 9:559–565
Dickenson JL (1997) Multiple mating, sperm competition, and cryptic female choice in the leaf beetles (Coleoptera: Chrysomelidae). In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 164–183
Dixon AFG, Agarwala BK (2002) Triangular fecundity function and ageing in ladybird beetles. Ecol Entomol 27:433–440
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
Eberhard WG (1997) Sexual selection by cryptic female choice in insects and arachnids. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 32–57
Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654
Haddrill PR, Shuker DM, Amos W, Majerus MEN, Mayes S (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Mol Ecol 17:3189–3197
Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proc R Soc Lond Ser B 270:1033–1040
Jiang XF, Luo LZ, Zhang L (2007) Relative fitness of near isogenic lines for melanic and typical forms of the oriental armyworm, Mythimna separata (Walker). Environ Entomol 36:1296–1301
Ma W, Chen L, Wang M, Li X (2008) Trade-offs between melanisation and life-history traits in Helicoverpa armigera. Ecol Entomol 33:37–44
Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, 338 pp
Martin-Vega D, Baz A (2011) Variation in the colour of the necrophagous fly, Prochyliza nigrimana (Diptera: Piophilidae): a case of seasonal polymorphism. Eur J Entomol 108:231–234
Michaud JP, Qureshi JA (2006) Reproductive diapause in Hippodamia convergens (Coleoptera: Coccinellidae) and its life history consequences. Biol Control 39:193–200
Milliken GA, Johnson DE (2009) Analysis of messy data, volume 1, designed experiments, 2nd edn. CRC Press, Boca Raton
Muggleton J (1975) Melanism in Adalia bipunctata (Coleoptera: Coccinellidae) and its relationship to atmospheric pollution. J Appl Ecol 12:451–464
Nahrung HF, Allen GR (2005) Maintenance of colour polymorphism in the leaf beetle Chrysophtharta agricola (Chapuis) (Coleoptera: Chrysomelidae: Paropsini). J Nat Hist 39:79–90
Nedved O, Honek A (2012) In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the Ladybird beetles (Coccinellidae). Wiley-Blackwell, Oxford, pp 54–109
Obata S (1987) Mating behaviour and sperm transfer in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl Entomol Zool 22:434–442
Osawa N, Nishida T (1992) Seasonal variation in elytra color polymorphism Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69:297–307
Parkash S, Singh S, Ramniwas S (2009) Seasonal changes in humidity level in the tropics impact body color polymorphism and desiccation resistance in Drosophila jambulina—evidence for melanism-desiccation hypothesis. J Insect Physiol 55:358–368
Quinones Pando FJ, Chavez Sanchez N, Tarango Rivero SH (2001) Effect of the time of availability of the male in the fecundity of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Fol Entomol Mex 40:47–52
Rhamhalinghan M (1998) The reproductive behaviour of Coccinella septempunctata L. var. Confusa Wiedmann (Coleoptera: Coccinellidae). J Adv Zool 19:17–21
SAS Institute (2013) The SAS System for Windows version 9.3. SAS Institute, Cary
Simmons LW, Siva-Jothy MT (1998) Sperm competition in insects: mechanisms and potential for selection. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 341–434
Sloggett JJ, Honek A (2012) Genetic studies. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the Ladybird beetles (Coccinellidae). Wiley-Blackwell, Oxford, pp 13–53
Stewart LA, Dixon AFG (1989) Why big species of ladybird beetles are not melanic. Funct Ecol 3:165–177
Tan CC, Li JC (1934) Inheritance of the elytral colour patterns in the lady-bird beetle, Harmonia axyridis. Am Nat 68:252–265
Thornhill R, Alcock J (1983) The evolution of insect mating systems. iUniverse.com, Lincoln
True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647
Ueno H (1994) Intraspecific variation of P2 value in a coccinellid beetle, Harmonia axyridis. J Ethol 12:169–174
Vargas G, Michaud JP, Nechols JR (2012) Larval food supply constrains female reproductive schedules in Hippodamia convergens (Coleoptera: Coccinellidae). Ann Entomol Soc Am (accepted)
Verhoog MD, Breuker CJ, Brakefield PM (1998) The influence of genes for melanism on the activity of the flour moth, Ephestia kuehniella. Anim Behav 56:683–688
Wang S, Michaud JP, Zhang RZ, Zhang F, Liu S (2009) Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecol Entomol 34:483–491
Acknowledgments
The authors thank G. Mishra for reviewing the manuscript. This work was funded by the National Basic Research Program of China (2012CB017359) and grant #31071731 from the National Science Foundation of China.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Su, W., Michaud, J.P., Xiaoling, T. et al. Melanism in a Chinese Population of Harmonia axyridis (Coleoptera: Coccinellidae): A Criterion for Male Investment with Pleiotropic Effects on Behavior and Fertility. J Insect Behav 26, 679–689 (2013). https://doi.org/10.1007/s10905-013-9384-6
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-013-9384-6