Abstract
Evolution of dispersal is affected by context-specific costs and benefits. One example is sex-biased dispersal in mammals and birds. While many such patterns have been described, the underlying mechanisms are poorly understood. Here, we study genetic and phenotypic traits that affect butterfly flight capacity and examine how these traits are related to dispersal in male and female Glanville fritillary butterflies (Melitaea cinxia). We performed two mark–recapture experiments to examine the associations of individuals’ peak flight metabolic rate (MRpeak) and Pgi genotype with their dispersal in the field. In a third experiment, we studied tethered flight in the laboratory. MRpeak was negatively correlated with dispersal distance in males but the trend was positive in females, and the interaction between MRpeak and sex was significant for long-distance dispersal. A similar but nonsignificant trend was found in relation to molecular variation at Pgi, which encodes a glycolytic enzyme: the genotype associated with high MRpeak tended to be less dispersive in males but more dispersive in females. The same pattern was repeated in the tethered flight experiment: the relationship between MRpeak and flight duration was positive in females but negative in males. These results suggest that females with high flight capacity are superior in among-population dispersal, which facilitates the spatial spreading of their reproductive effort. In contrast, males with high flight capacity may express territorial behaviour, and thereby increase the number of matings, whereas inferior males may be forced to disperse. Thus, flight capacity has opposite associations with dispersal rate in the two sexes.
Similar content being viewed by others
References
Becker BJ (1994) Combining significance levels. In: Cooper HJ, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, pp 215–230
Bergman M, Wiklund C (2009) Differences in mate location behaviours between residents and nonresidents in a territorial butterfly. Anim Behav 78:1161–1167
Bergman M, Gotthard K, Berger D, Olofsson M, Kemp DJ, Wiklund C (2007) Mating success of resident versus non-resident males in a territorial butterfly. Proc R Soc Lond B 274:1659–1665
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
Berwaerts K, Matthysen E, Van Dyck H (2008) Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment. Evolution 62:2525–2533
Davies NB (1978) Territorial defence in speckled wood butterfly (Pararge aegeria)—resident always wins. Anim Behav 26:138–147
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Gros A, Hovestadt T, Poethke HJ (2008) Evolution of sex-biased dispersal: the role of sex-specific dispersal costs, demographic stochasticity, and inbreeding. Ecol Modell 219:226–233
Haag CR, Saastamoinen M, Marden JH, Hanski I (2005) A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc R Soc Lond B 272:2449–2456
Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. Plos Biol 4:719–726
Hanski I, Peltonen A, Kaski L (1991) Natal dispersal and social dominance in the common shrew Sorex araneus. Oikos 62:48–58
Hanski I, Erälahti C, Kankare M, Ovaskainen O, Sirén H (2004) Variation in migration propensity among individuals maintained by landscape structure. Ecol Lett 7:958–966
Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. J Anim Ecol 75:91–100
Heino M, Hanski I (2001) Evolution of migration rate in a spatially realistic metapopulation model. Am Nat 157:495–511
Hill JK, Thomas CD, Blakeley DS (1999a) Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia 121:165–170
Hill JK, Thomas CD, Lewis OT (1999b) Flight morphology in fragmented populations of a rare British butterfly, Hesperia comma. Biol Conserv 87:277–283
Ide JY (2002) Seasonal changes in the territorial behaviour of the Satyrine butterfly Lethe diana are mediated by temperature. J Ethol 20:71–78
Kemp DJ, Rutowski RL (2001) Spatial and temporal patterns of territorial mate locating behaviour in Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae). J Nat Hist 35:1399–1411
Kemp DJ, Wiklund C (2001) Fighting without weaponry: a review of male–male contest competition in butterflies. Behav Ecol Sociobiol 49:429–442
Kemp DJ, Wiklund C, Van Dyck H (2006) Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance. Behav Ecol Sociobiol 59:403–411
Kuussaari M, Nieminen M, Hanski I (1996) An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J Anim Ecol 65:791–801
Lawson Handley LJ, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578
Marden JH, Cobb JR (2004) Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites. Anim Behav 68:857–865
Marden JH, Rollins RA (1994) Assessment of energy reserves by damselflies engaged in aerial contests for mating territories. Anim Behav 48:1023–1030
Martinez-Lendech N, Cordoba-Aguilar A, Serrano-Meneses MA (2007) Body size and fat reserves as possible predictors of male territorial status and contest outcome in the butterfly Eumaeus toxea Godart (Lepidoptera: Lycaenidae). J Ethol 25:195–199
Merckx T, Van Dyck H (2005) Mate location behaviour of the butterfly Pararge aegeria in woodland and fragmented landscapes. Anim Behav 70:411–416
Niitepõld K (2010) Genotype by temperature interactions in the metabolic rate of the Glanville fritillary butterfly. J Exp Biol 213:1042–1048
Niitepõld K et al (2009) Flight metabolic rate and Pgi genotype influence butterfly dispersal rate in the field. Ecology 90:2223–2232
Orsini L, Wheat CW, Haag CR, Kvist J, Frilander MJ, Hanski I (2009) Fitness differences associated with Pgi SNP genotypes in the Glanville fritillary butterfly (Melitaea cinxia). J Evol Biol 22:367–375
Otronen M (1995) Energy reserves and mating success in males of the yellow dung fly, Scathophaga stercoraria. Funct Ecol 9:683–688
Ovaskainen O et al (2008) Tracking butterfly movements with harmonic radar reveals an effect of population age on movement distance. Proc Natl Acad Sci USA 105:19090–19095
Peixoto PEC, Benson WW (2008) Body mass and not wing length predicts territorial success in a tropical satyrine butterfly. Ethology 114:1069–1077
Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127
Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803
Roff DA, Fairbairn DJ (2007) The evolution and genetics of migration in insects. Bioscience 57:155–164
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253
Saastamoinen M (2007a) Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecol Entomol 32:235–242
Saastamoinen M (2007b) Mobility and lifetime fecundity in new versus old populations of the Glanville fritillary butterfly. Oecologia 153:569–578
Saastamoinen M (2008) Heritability of dispersal rate and other life history traits in the Glanville fritillary butterfly. Heredity 100:39–46
Saastamoinen M, Hanski I (2008) Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am Nat 171:E701–E712
Scott JA (1974) Mate-locating behavior of butterflies. Am Midl Nat 91:103–117
Singer MC, Hanski I (2004) Dispersal behavior and evolutionary metapopulation dynamics. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, New York, pp 181–198
Van Dyck H, Matthysen E (1999) Habitat fragmentation and insect flight: a changing ‘design’ in a changing landscape? Trends Ecol Evol 14:172–174
Van Dyck H, Matthysen E, Dhondt A (1997) Mate-locating strategies are related to relative body length and wing colour in the speckled wood butterfly Pararge aegeria. Ecol Entomol 22:116–120
Wahlberg N (2000) Comparative descriptions of the immature stages and ecology of five Finnish melitaeine butterfly species (Lepidoptera: Nymphalidae). Entomol Fenn 11:167–174
Watt WB (1983) Adaptation at specific loci. II. Demographic and biochemical elements in the maintenance of the Colias PGI polymorphism. Genetics 103:691–724
Watt WB, Wheat CW, Meyer EH, Martin JF (2003) Adaptation at specific loci. VII. Natural selection, dispersal and the diversity of molecular-functional variation patterns among butterfly species complexes (Colias: Lepidoptera, Pieridae). Mol Ecol 12:1265–1275
Wickman PO (1992) Sexual selection and butterfly design—a comparative study. Evolution 46:1525–1536
Wickman PO, Wiklund C (1983) Territorial defense and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim Behav 31:1206–1216
Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–230
Zheng CZ, Ovaskainen O, Hanski I (2009) Modelling single nucleotide effects in phosphoglucose isomerase on dispersal in the Glanville fritillary butterfly: coupling of ecological and evolutionary dynamics. Philos Trans R Soc Lond B 364:1519–1532
Acknowledgments
We thank J.H. Marden for comments and providing the respirometry equipment. We wish to thank S. Buckland for advice on randomisation tests. S. Ikonen, J. Kallio, M. Kekkonen, P. Väisänen and M. Ylivinkka are thanked for their assistance in the field. We are grateful to R. Nesbit and J. Chapman for their hard work in the tethered flight experiment. We thank T. Nyman and L. Orsini for help and advice on genotyping. W. Watt and H. Van Dyck are thanked for comments on previous versions of the manuscript. We thank the inhabitants of the Husö Island for their hospitality and for sustaining traditional agriculture in the Åland archipelago. Financial support was provided by the University of Helsinki, the Academy of Finland (Finnish CoE Programme 2000–2005, 2006–2011, grant numbers 131155, 38604 and 44887), the U.S. National Science Foundation (EF-0412651) and the European Research Council (AdG number 232826 to IH). P.J.H. received funding from the Academy of Finland (grant 116941). The experiments reported here comply with the current law in the United Kingdom and Finland.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jérome Casas.
K. Niitepõld and A. L.K. Mattila contributed equally to this work.
Rights and permissions
About this article
Cite this article
Niitepõld, K., Mattila, A.L.K., Harrison, P.J. et al. Flight metabolic rate has contrasting effects on dispersal in the two sexes of the Glanville fritillary butterfly. Oecologia 165, 847–854 (2011). https://doi.org/10.1007/s00442-010-1886-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1886-8