Flight-induced changes in gene expression in the Glanville fritillary butterfly.
Insect flight is one of the most energetically demanding activities in the animal kingdom, yet for many insects flight is necessary for reproduction and foraging. Moreover, dispersal by flight is essential for the viability of species living in fragmented landscapes. Here, working on the Glanville fritillary butterfly (Melitaea cinxia), we use transcriptome sequencing to investigate gene expression changes caused by 15 min of flight in two contrasting populations and the two sexes. Male butterflies and individuals from a large metapopulation had significantly higher peak flight metabolic rate (FMR) than female butterflies and those from a small inbred population. In the pooled data, FMR was significantly positively correlated with genome-wide heterozygosity, a surrogate of individual inbreeding. The flight experiment changed the expression level of 1513 genes, including genes related to major energy metabolism pathways, ribosome biogenesis and RNA processing, and stress and immune responses. Males and butterflies from the population with high FMR had higher basal expression of genes related to energy metabolism, whereas females and butterflies from the small population with low FMR had higher expression of genes related to ribosome/RNA processing and immune response. Following the flight treatment, genes related to energy metabolism were generally down-regulated, while genes related to ribosome/RNA processing and immune response were up-regulated. These results suggest that common molecular mechanisms respond to flight and can influence differences in flight metabolic capacity between populations and sexes.
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 9), Helsinki, Finland.
Jouni
J
Kvist
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Anniina L K
AL
Mattila
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 9), Helsinki, Finland.|Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.|Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 4), Helsinki, Finland.
Panu
P
Somervuo
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Virpi
V
Ahola
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 9), Helsinki, Finland.|Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.|Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 4), Helsinki, Finland.
Patrik
P
Koskinen
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 4), Helsinki, Finland.
Lars
L
Paulin
Department of Computer Science and Helsinki Institute for Information Technology HIIT, University of Helsinki, P.O. Box 68 (Gustaf Hällströmin katu 2b), Helsinki, Finland.
Leena
L
Salmela
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Toby
http://orcid.org/0000-0002-5501-4691
T
Fountain
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Pasi
P
Rastas
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Annukka
A
Ruokolainen
Science for Life Laboratory, Department of Biosciences and Nutrition, Karolinska Institutet (Hälsovägen 7), SE-14157, Huddinge, Sweden.
Minna
M
Taipale
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.|Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 4), Helsinki, Finland.
Liisa
L
Holm
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 4), Helsinki, Finland.
Petri
P
Auvinen
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Rainer
R
Lehtonen
Institute of Biotechnology, University of Helsinki, P.O. Box 56 (Viikinkaari 9), Helsinki, Finland.
Mikko J
MJ
Frilander
Department of Biosciences, University of Helsinki, P.O. Box 65 (Viikinkaari 1), Helsinki, FI-00014, Finland.
Ilkka
I
Hanski
D000818:Animals; D002080:Butterflies / Q000235:genetics* / Q000502:physiology; D004734:Energy Metabolism / Q000235:genetics; D005260:Female; D005387:Finland; D005426:Flight, Animal; D015870:Gene Expression; D008297:Male; D008969:Molecular Sequence Data; D020641:Polymorphism, Single Nucleotide; D017423:Sequence Analysis, RNA; D012727:Sex Characteristics; D059467:Transcriptome
energy metabolism; flight metabolic rate; gene expression; genetic load; immune response; insect flight; ribosome biogenesis; small population