Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-04T21:03:30.707Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexual selection drives the evolution of limb regeneration in Harmonia axyridis (Coleoptera: Coccinellidae)

Published online by Cambridge University Press:  30 January 2015

S. Wang ,
X.L. Tan ,
J.P. Michaud ,
Z.K. Shi  and
F. Zhang
S. Wang
Affiliation:
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
X.L. Tan
Affiliation:
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
J.P. Michaud*
Affiliation:
Department of Entomology, Kansas State University, Agricultural Research Center-Hays, Hays, Kansas, USA
Z.K. Shi
Affiliation:
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
F. Zhang
Affiliation:
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
*
*Author for correspondence Phone: 785-625-3425 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

When Harmonia axyridis larvae were subjected to amputation of a foreleg in the fourth instar, 83% survived and, of these, 75% regenerated the leg during pupation. Regenerators pupated at heavier weights than controls (unoperated) or non-regenerators, and spent longer in pupation. Regenerated males were preferred by females in choice tests and produced more viable progeny than control males. Unregenerated males were less preferred by females, copulated for shorter periods than control males, and reduced female fecundity. Amputation diminished beneficial paternal effects, whether males regenerated or not, resulting in progeny with slower development and smaller adult body mass relative to control paternity. Progeny of unregenerated males had lower survival and body mass, whether male or female, confirming that regeneration was an honest signal of mate quality. When offspring had a foreleg amputated, a regenerated paternity yielded higher survival than control paternity, but similar rates of regeneration, whereas an unregenerated paternity yielded lower rates of survival and leg regeneration than control paternity. Regenerating beetles were twice as likely to be melanic as non-regenerating or control beetles, suggesting pleiotropic effects of melanism on processes involved in regeneration. This is the first report of complete limb regeneration by a holometabolous insect in the pupal stage, and the first example of sexual selection for regenerative capacity.

Keywords

body sizedevelopmentfemale choicefitnessmelanismpaternal effects
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 2 , April 2015 , pp. 245 - 252
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alibardi, L. (2012) Observations on FGF immunoreactivity in the regenerating tail blastema, and in the limb and tail scars of lizard suggest that FGFs are required for regeneration. Journal of Zoology 142, 23–38.Google Scholar
Benelli, G., Donati, E., Romano, D., Stefanini, C., Messing, R.H. & Canale, A. (2015) Lateralisation of aggressive displays in a tephritid fly. Science of Nature (in press) DOI: 01/2015; DOI: 10.1007/s00114-014-1251-6.CrossRefGoogle Scholar
Bezzerides, A.L., McGraw, K.J., Parker, R.S. & Husseini, J. (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis . Behavioral Ecology and Sociobiology 61, 1401–1408.CrossRefGoogle Scholar
Brockes, J.P. & Gates, P.B. (2014) Mechanisms underlying vertebrate limb regeneration: lessons from the salamander. Biochemical Society Transactions 42, 625–630.CrossRefGoogle ScholarPubMed
Cuervo, R., Hernandez-Martinez, R., Chimal-Monroy, J., Merchant-Larios, H. & Covarrubias, L. (2012) Full regeneration of the tribasal Polypterus fin. Proceedings of the National Academy of Sciences 109, 3838–3843.CrossRefGoogle ScholarPubMed
Daloze, D., Braekman, J.C. & Pasteels, J.M. (1995) Ladybird defence alkaloids: structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5/6, 173–183.Google Scholar
Frasnelli, E., Vallortigara, G. & Rogers, L. (2012) Left-right asymmetries of behaviour and nervous system in invetebrates. Neuroscience and Biobehavioral Reviews 36, 1273–1291.CrossRefGoogle Scholar
Grafen, A. (1990a) Sexual selection unhandicapped by the Fisher process. Journal of Theoretical Biology 144, 475–516.CrossRefGoogle ScholarPubMed
Grafen, A. (1990b) Biological signals as handicaps. Journal of Theoretical Biology 144, 517–546.Google ScholarPubMed
Haulotte, E., Laurent, P. & Braekman, J.C. (2012) Biosynthesis of defensive coccinellidae alkaloids: incorporation of fatty acids in adaline, coccinelline, and harmonine. European Journal of Organic Chemistry 10, 1907–1912.CrossRefGoogle Scholar
Hemptinne, J.L. & Dixon, A.F.G. (2000) Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera, Coccinellidae)? A short review. European Journal of Entomology 97, 443–447.CrossRefGoogle Scholar
Hemptinne, J.L., Lognay, G. & Dixon, A.F.G. (1998) Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. Journal of Insect Physiology 44, 1163–1171.CrossRefGoogle Scholar
Joseph, S.B., Snyder, W.E. & Moore, A.J. (1999). Cannibalizing Harmonia axyridis (Coleoptera: Coccinellidae) larvae use endogenous cues to avoid eating relatives. Journal of Evolutionary Biology 12, 792–797.CrossRefGoogle Scholar
Karuppanan, U. (1998) Regeneration in the limbs of mantids (Dictyoptera: Mantidae). Journal of Ecobiology 10, 27–36.Google Scholar
Katsanis, A., Babendreier, D., Nentwig, W. & Kenis, M. (2013) Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species. BioControl 58, 73–83.CrossRefGoogle Scholar
Knobloch, C.A. & Steel, C.G.H. (1988) Interactions between limb regeneration and ecdysteroid titers in last larval instar Rhodnius prolixus (Hemiptera). Journal of Insect Physiology 34, 507–514.CrossRefGoogle Scholar
Koch, R.L. (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3, 32.CrossRefGoogle ScholarPubMed
Kumar, A., Nevill, G., Brockes, J.P. & Forge, A. (2010) A comparative study of gland cells implicated in the nerve dependence of salamander limb regeneration. Journal of Anatomy 217, 16–25.CrossRefGoogle ScholarPubMed
Lakes, R. & Mucke, A. (1989) Regeneration of the foreleg tibia and tarsi of Ephippiger ephippiger (Orthoptera: Tettigoniidae). Journal of Experimental Zoology 250, 176–187.CrossRefGoogle Scholar
Laurent, P., Braekman, J.C., Daloze, D. & Pasteels, J.M. (2002) In vitro production of adaline and coccinelline, two defensive alkaloids from ladybird beetles (Coleoptera: Coccinellidae). Insect Biochemical and Molecular Biology 32, 1017–1023.CrossRefGoogle ScholarPubMed
Lee, A.K., Sze, C.C., Kim, E.R. & Suzuki, Y. (2013) Developmental coupling of larval and adult stages in a complex life cycle: insights from limb regeneration in the flour beetle, Tribolium castaneum . Evodevo 4, 20. doi: 10.1186/2041-9139-4-20.CrossRefGoogle Scholar
Li, H., Zhang, X.H. & Na, J. (2007) The hind leg regeneration in the nymphs of Gryllus bimaculata . Chinese Bulletin of Entomology 44, 419–422.Google Scholar
Lobo, D., Beane, W.S. & Levin, M. (2012) Modeling planarian regeneration: a primer for reverse-engineering the worm. PLoS Comparative Biology 8, e100248.CrossRefGoogle ScholarPubMed
Martini, X., Haccou, P., Olivieri, I. & Hemptinne, J.L. (2009) Evolution of cannibalism and female's response to oviposition-deterring pheromone in aphidophagous predators. Journal of Animal Ecology 78, 964–972.CrossRefGoogle ScholarPubMed
Martini, X., Dixon, A.F.G. & Hemptinne, J.L. (2013) The effect of relatedness on the response of Adalia bipunctata L. to oviposition deterring cues. Bulletin of Entomological Research 103, 14–19.CrossRefGoogle ScholarPubMed
Michaud, J.P. (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native ladybeetle, Cycloneda sanguinea . Environmental Entomology 31, 827–835.CrossRefGoogle Scholar
Michaud, J.P. (2003) A comparative study of larval cannibalism in three species of ladybird. Ecological Entomology 28, 92–101.CrossRefGoogle Scholar
Michaud, J.P., Bista, M., Mishra, G. & Omkar, (2013) Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development. Bulletin of Entomological Research 103, 570–577.CrossRefGoogle ScholarPubMed
Mirhosseini, M.A., Michaud, J.P., Jalali, M.A. & Ziaaddini, M. (2014) Paternal effects correlate with female reproductive stimulation in a polyandrous ladybird, Cheilomenes sexmaculata . Bulletin of Entomological Research 104, 480–485.CrossRefGoogle Scholar
Mitten, E.K., Jing, D. & Suzuki, Y. (2012) Matrix metalloproteinases (MMPs) are required for wound closure and healing during larval leg regeneration in the flour beetle, Tribolium castaneum . Insect Biochemical and Molecular Biology 42, 854–864.CrossRefGoogle ScholarPubMed
Murciano, C., Fernandez, T.D., Duran, I., Maseda, D., Ruiz-Sanchez, J., Becerra, J., Akimenko, M.A. & Mari-Beffa, M. (2002) Ray-interray interactions during fin regeneration of Danio rerio . Developmental Biology 252, 214–224.CrossRefGoogle ScholarPubMed
Nacu, E. & Tanaka, E. (2011) Limb regeneration: a new development? Annual Review of Cell and Developmental Biology 27, 409–440.CrossRefGoogle ScholarPubMed
Osawa, N. & Nishida, T. (1992) Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69, 297–307.CrossRefGoogle Scholar
Passamaneck, Y.J. & Martindale, M.Q. (2012) Cell proliferation is necessary for the regeneration of oral structures in the anthozoan cnidarian Nematostella vectensis . BMC Developmental Biology 12, 34. doi: 10.1186/1471-213X-12-34.CrossRefGoogle ScholarPubMed
Pell, J.K., Baverstock, J., Roy, H.E., Ware, R.L. & Majerus, M.E.N. (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53, 147–168.CrossRefGoogle Scholar
Perry, J.C., Sharpe, D.M.T. & Rowe, L. (2009) Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle. Animal Behaviour 77, 743–748.CrossRefGoogle Scholar
Rogers, J.L. & Andrew, R.J. (2002) Comparative vertebrate lateralization. Cambridge University Press.CrossRefGoogle Scholar
Roy, H.E. & Wajnberg, E. (2008) From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl 53, 1–4.CrossRefGoogle Scholar
Satoh, A., Graham, G.M.C., Bryant, S.V. & Gardiner, D.M. (2008) Neurotrophic regulation of epidermal dedifferentiation during wound healing and limb regeneration in the axolotl (Ambystoma mexicanum). Developmental Biology 319, 321–335.CrossRefGoogle ScholarPubMed
Satoh, A., Bryant, S.V. & Gardiner, D.M. (2012) Nerve signaling regulates basal keratinocyte proliferation in the blastema apical epithelial cap in the axolotl (Ambystoma mexicanum). Developmental Biology 366, 374–381.CrossRefGoogle ScholarPubMed
Selin, N.I. (2003) Limb regeneration in male tanner crabs Chionoecetes bairdi and Ch. opilio . Biologiya Morya (Vladivostok) 29, 198–201.Google Scholar
Shah, M., Namigai, E. & Suzuki, Y. (2011) The role of canonical Wnt signaling in leg regeneration and metamorphosis in the red flour beetle Tribolium castaneum . Mechanisms of Development 4, 342–400.CrossRefGoogle Scholar
Shock, B.C., Foran, C.M. & Stueckle, T.A. (2009) Effects of salinity stress on survival, metabolism, limb regeneration, and ecdysis in Uca pugnax . Journal of Crustacean Biology 29, 293–301.CrossRefGoogle Scholar
Singh, A., Kango-Singh, M., Parthasarathy, R. & Gopinathan, K.P. (2007) Larval legs of mulberry silkworm Bombyx mori are prototypes for the adult legs. Genesis 45, 169–176.CrossRefGoogle ScholarPubMed
Tan, X., Zhao, J., Wang, S. & Zhang, F. (2014) Optimization and evaluation of microencapsulated artificial diet for mass rearing the predatory ladybird Propylea japonica (Coleoptera: Coc-cinellidae). Insect Science doi: 10.1111/1744-7917.12098.Google Scholar
Tanaka, A., Ohtake-Hashiguchi, M. & Ogawa, E. (1987) Repeated regeneration of the German cockroach legs. Growth 51, 282–300.Google ScholarPubMed
Truby, P.R. (1983) Blastema formation and cell division during cockroach limb regeneration. Journal of Embryology and Experimental Morphology 75, 151–164.Google ScholarPubMed
True, J.R. (2003) Insect melanism: the molecules matter. Trends in Ecology and Evolution 18, 640–647.CrossRefGoogle Scholar
Ueno, H., Sato, Y. & Tusuchida, K. (1998) Colour-associated mating success in a polymorphic ladybird beetle, Harmonia axyridis . Functional Ecology 12, 757–761.CrossRefGoogle Scholar
Wang, S., Michaud, J.P., Zhang, R., Zhang, F. & Liu, S. (2009) Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecological Entomology 34, 483–494.Google Scholar
Wang, S., Michaud, J.P., Tan, X.L., Murray, L. & Zhang, F. (2013) Melanism in a Chinese population of Harmonia axyridis (Coleoptera: Coccinellidae): a criterion for male investment with pleiotropic effects on behavior and fertility. Journal of Insect Behavior 26, 679–689.Google Scholar
Wigglesworth, V.B. (1965) The Principles of Insect Physiology. 6th edn. 741 pp. London, Methuen.Google Scholar
Wolpert, L. (2011) Positional information and patterning revisited. J Theor Biol. 269(1), 359–65.CrossRefGoogle ScholarPubMed
Yanez-Rivera, B. & Mendez, N. (2014) Regeneration in the stinging fireworm Eurythoe (Annelida): lipid and triglyceride evaluation. Journal of Experimental Marine Biology and Ecology 459, 137–143.CrossRefGoogle Scholar
Zahavi, A. (1975) Mate selection – a selection for a handicap. Journal of Theoretical Biology 53, 205–214.CrossRefGoogle ScholarPubMed
Zahavi, A. & Zahavi, A. (1997) The Handicap Principle: A Missing Piece of Darwin's Puzzle. Oxford, Oxford University Press.CrossRefGoogle Scholar