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Transcriptome analysis reveals signature of adaptation to landscape fragmentation

Somervuo, Panu ; Kvist, Jouni ; Ikonen, Suvi ; Auvinen, Petri ; Paulin, Lars ; Koskinen, Patrik ; Holm, Liisa ; Taipale, Minna ; Duplouy, Anne LU and Ruokolainen, Annukka , et al. (2014) In PLoS ONE 9(7).
Abstract

We characterize allelic and gene expression variation between populations of the Glanville fritillary butterfly (Melitaea cinxia) from two fragmented and two continuous landscapes in northern Europe. The populations exhibit significant differences in their life history traits, e.g. butterflies from fragmented landscapes have higher flight metabolic rate and dispersal rate in the field, and higher larval growth rate, than butterflies from continuous landscapes. In fragmented landscapes, local populations are small and have a high risk of local extinction, and hence the long-term persistence at the landscape level is based on frequent re-colonization of vacant habitat patches, which is predicted to select for increased dispersal rate.... (More)

We characterize allelic and gene expression variation between populations of the Glanville fritillary butterfly (Melitaea cinxia) from two fragmented and two continuous landscapes in northern Europe. The populations exhibit significant differences in their life history traits, e.g. butterflies from fragmented landscapes have higher flight metabolic rate and dispersal rate in the field, and higher larval growth rate, than butterflies from continuous landscapes. In fragmented landscapes, local populations are small and have a high risk of local extinction, and hence the long-term persistence at the landscape level is based on frequent re-colonization of vacant habitat patches, which is predicted to select for increased dispersal rate. Using RNA-seq data and a common garden experiment, we found that a large number of genes (1,841) were differentially expressed between the landscape types. Hexamerin genes, the expression of which has previously been shown to have high heritability and which correlate strongly with larval development time in the Glanville fritillary, had higher expression in fragmented than continuous landscapes. Genes that were more highly expressed in butterflies from newly-established than old local populations within a fragmented landscape were also more highly expressed, at the landscape level, in fragmented than continuous landscapes. This result suggests that recurrent extinctions and re-colonizations in fragmented landscapes select a for specific expression profile. Genes that were significantly up-regulated following an experimental flight treatment had higher basal expression in fragmented landscapes, indicating that these butterflies are genetically primed for frequent flight. Active flight causes oxidative stress, but butterflies from fragmented landscapes were more tolerant of hypoxia. We conclude that differences in gene expression between the landscape types reflect genomic adaptations to landscape fragmentation.

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PLoS ONE
volume
9
issue
7
article number
e101467
pages
12 pages
publisher
Public Library of Science
external identifiers
  • scopus:84903786693
  • pmid:24988207
ISSN
1932-6203
DOI
10.1371/journal.pone.0101467
language
English
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no
id
545e5d22-2337-49b2-a347-cf382c039421
date added to LUP
2018-11-14 16:23:23
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2020-01-16 03:37:07
@article{545e5d22-2337-49b2-a347-cf382c039421,
  abstract     = {<p>We characterize allelic and gene expression variation between populations of the Glanville fritillary butterfly (Melitaea cinxia) from two fragmented and two continuous landscapes in northern Europe. The populations exhibit significant differences in their life history traits, e.g. butterflies from fragmented landscapes have higher flight metabolic rate and dispersal rate in the field, and higher larval growth rate, than butterflies from continuous landscapes. In fragmented landscapes, local populations are small and have a high risk of local extinction, and hence the long-term persistence at the landscape level is based on frequent re-colonization of vacant habitat patches, which is predicted to select for increased dispersal rate. Using RNA-seq data and a common garden experiment, we found that a large number of genes (1,841) were differentially expressed between the landscape types. Hexamerin genes, the expression of which has previously been shown to have high heritability and which correlate strongly with larval development time in the Glanville fritillary, had higher expression in fragmented than continuous landscapes. Genes that were more highly expressed in butterflies from newly-established than old local populations within a fragmented landscape were also more highly expressed, at the landscape level, in fragmented than continuous landscapes. This result suggests that recurrent extinctions and re-colonizations in fragmented landscapes select a for specific expression profile. Genes that were significantly up-regulated following an experimental flight treatment had higher basal expression in fragmented landscapes, indicating that these butterflies are genetically primed for frequent flight. Active flight causes oxidative stress, but butterflies from fragmented landscapes were more tolerant of hypoxia. We conclude that differences in gene expression between the landscape types reflect genomic adaptations to landscape fragmentation.</p>},
  author       = {Somervuo, Panu and Kvist, Jouni and Ikonen, Suvi and Auvinen, Petri and Paulin, Lars and Koskinen, Patrik and Holm, Liisa and Taipale, Minna and Duplouy, Anne and Ruokolainen, Annukka and Saarnio, Suvi and Sireń, Jukka and Kohonen, Jukka and Corander, Jukka and Frilander, Mikko J. and Ahola, Virpi and Hanski, Ilkka},
  issn         = {1932-6203},
  language     = {eng},
  month        = {07},
  number       = {7},
  publisher    = {Public Library of Science},
  series       = {PLoS ONE},
  title        = {Transcriptome analysis reveals signature of adaptation to landscape fragmentation},
  url          = {http://dx.doi.org/10.1371/journal.pone.0101467},
  doi          = {10.1371/journal.pone.0101467},
  volume       = {9},
  year         = {2014},
}