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The transcriptional landscape of seasonal coat colour moult in the snowshoe hare

  • Mafalda S. Ferreira
  • , Paulo C. Alves
  • , Colin M. Callahan
  • , João P. Marques
  • , L. Scott Mills
  • , Jeffrey M. Good
  • , José Melo-Ferreira
  • University of Porto
  • University of Montana

Research output: Contribution to journalArticlepeer-review

25 Scopus citations

Abstract

Seasonal coat colour change is an important adaptation to seasonally changing environments but the evolution of this and other circannual traits remains poorly understood. In this study, we use gene expression to understand seasonal coat colour moulting in wild snowshoe hares (Lepus americanus). We used hair colour to follow the progression of the moult, simultaneously sampling skin from three moulting stages in hares collected during the peak of the spring moult from white winter to brown summer pelage. Using RNA sequencing, we tested whether patterns of expression were consistent with predictions based on the established phases of the hair growth cycle. We found functionally consistent clustering across skin types, with 766 genes differentially expressed between moult stages. “White” pelage showed more differentially expressed genes that were upregulated relative to other skin types, involved in the transition between late telogen (quiescent stage) and the onset of anagen (proliferative stage). Skin samples from transitional “intermediate” and “brown” pelage were transcriptionally similar and resembled the regressive transition to catagen (regressive stage). We also detected differential expression of several key circadian clock and pigmentation genes, providing important means to dissect the bases of alternate seasonal colour morphs. Our results reveal that pelage colour is a useful biomarker for seasonal change but that there is a consistent lag between the main gene expression waves and change in visible coat colour. These experiments establish that developmental sampling from natural populations of nonmodel organisms can provide a crucial resource to dissect the genetic basis and evolution of complex seasonally changing traits.

Original languageEnglish
Pages (from-to)4173-4185
Number of pages13
JournalMolecular Ecology
Volume26
Issue number16
DOIs
StatePublished - Aug 2017

Funding

Funding information Fundação para a Ciência e a Tecnologia (FEDER-COMPETE and Portuguese National Funds), Grant/Award Number: PTDC/BIA-EVF/115069/2009; Fundação para a Ciência e a Tecnologia (National funds), Grant/Award Number: PTDC/BIA-EVF/1624/2014, FCT-ANR/BIA-EVF/0250/2012; Fundação para a Ciência e a Tecnologia (POPH-QREN-ESF and Portuguese MCTES), Grant/Award Number: IF/00033/2014/CP1256/CT0005, PD/BD/108131/2015, SFRH/BD/115089/2016; ON.2 - O Novo Norte (National Strategic Reference Framework and the ERDF), Grant/Award Number: Genomics and Evolutionary Biology; University of Montana; National Science Foundation Division of Environmental Biology, Grant/Award Number: 0841884; Fundação Luso-Americana para o Desenvolvimento; M.J. Murdock Charitable Trust, Grant/Award Number: University of Montana Genomics Core; NIH Instrumentation, Grant/Award Number: S10RR029668 and S10RR027303; European Union FP7, Grant/Award Number: 286431. The authors would like to thank Fernando Seixas, Liliana Farelo, Sara Lado, Dan Vanderpool, Sara Keeble and members of the Good laboratory for helpful discussions on the generation and analysis of data. Financial support was partially obtained from FCT, Fundação para a Ciência e a Tecnologia: project grant “CRYPSIS” PTDC/BIA-EVF/115069/2009 (cofunded by FEDER through the COMPETE program and Portuguese National funds) funded library preparation, sequencing and preliminary analyses, while final analyses were performed in the framework of project grant “CHANGE” PTDC/BIA-EVF/1624/2014 (funded by Portuguese National Funds through the FCT). M.S.F and J.P.M. were supported by Portuguese National Funds through FCT (project grant “HybridAdapt” FCT-ANR/BIA-EVF/0250/2012) and by POPH-QREN funds from ESF and Portuguese MCTES/FCT (PD/BD/108131/2015 PhD grant in the scope of BIODIV PhD programme at Faculty of Sciences, University of Porto, to M.S.F., and SFRH/BD/115089/2016 PhD grant to J.P.M.). J.M.F. was supported by FCT Investigator grant IF/00033/2014/CP1256/CT0005 (POPH-QREN funds from ESF and Portuguese MCTES/FCT). Support was additionally obtained from project “Genomics and Evolutionary Biology” (cofunded by North Portugal Regional Operational Programme 2007/2013—ON.2—O Novo Norte—under the National Strategic Reference Framework and the European Regional Development Fund), University of Montana research funds to J.M.G., FLAD (Luso-American Foundation) travel grants to P.C.A, J.M.F and M.S.F., and the National Science Foundation Division of Environmental Biology Grant 0841884 to L.S.M. Additional instrumentation, laboratory and computational support was provided by the University of Montana Genomics Core, supported by a grant from the M.J. Murdock Charitable Trust, the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303, and CIBIO NEW-GEN sequencing platform, supported by European Union's Seventh Framework Programme for research, technological development and demonstration under grant agreement no. 286431.

FundersFunder number
FCT-ANR/BIA-EVF/0250/2012, PTDC/BIA-EVF/1624/2014, PTDC/BIA-EVF/115069/2009
0841884
PD/BD/108131/2015 PhD
S10RR027303, S10RR029668
286431
PD/BD/108131/2015, SFRH/BD/115089/2016, IF/00033/2014/CP1256/CT0005
Universidade Federal de Ciências da Saúde de Porto AlegreSFRH/BD/115089/2016 PhD

    UN SDGs

    This output contributes to the following UN Sustainable Development Goals (SDGs)

    1. SDG 13 - Climate Action
      SDG 13 Climate Action

    Keywords

    • Lepus americanus
    • RNA sequencing
    • climate change
    • gene expression
    • seasonal coat colour change

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