Inverse European Latitudinal Cline at the timeless Locus of Drosophila melanogaster Reveals Selection on a Clock Gene: Population Genetics of ls-tim

Valeria Zonato, Stefano Vanin, Rodolfo Costa, Eran Tauber, Charalambos P. Kyriacou

Research output: Contribution to journalArticlepeer-review

Abstract

The spread of adaptive genetic variants in populations is a cornerstone of evolutionary theory but with relatively few biologically well-understood examples. Previous work on the ls-tim variant of timeless, which encodes the light-sensitive circadian regulator in Drosophila melanogaster, suggests that it may have originated in southeastern Italy. Flies characterized by the new allele show photoperiod-related phenotypes likely to be adaptive in seasonal environments. ls-tim may be spreading from its point of origin in Italy by directional selection, but there are alternative explanations for its observed clinal geographical distribution, including balancing selection and demography. From population analyses of ls-tim frequencies collected on the eastern side of the Iberian Peninsula, we show that ls-tim frequencies are inverted compared with those in Italy. This pattern is consistent with a scenario of directional selection rather than latitude-associated balancing selection. Neutrality tests further reveal the signature of directional selection at the ls-tim site, which is reduced a few kb pairs either side of ls-tim. A reanalysis of allele frequencies from a large number of microsatellite loci do not demonstrate any frequent ls-tim-like spatial patterns, so a general demographic effect or population expansion from southeastern Italy cannot readily explain current ls-tim frequencies. Finally, a revised estimate of the age of ls-tim allele using linkage disequilibrium and coalescent-based approaches reveals that it may be only 300 to 3000 years old, perhaps explaining why it has not yet gone to fixation. ls-tim thus provides a rare temporal snapshot of a new allele that has come under selection before it reaches equilibrium.

Original languageEnglish
Pages (from-to)15-23
Number of pages9
JournalJournal of Biological Rhythms
Volume33
Issue number1
DOIs
StatePublished - 1 Feb 2018

Bibliographical note

Funding Information:
This work was funded by grants from the European Community (the 6th Framework Project EUCLOCK No. 018741 and the 7th Framework Project INsecTIME No. 316790) to R.C. and C.P.K., a NERC and a BBSRC grant to E.T. and C.P.K. We thank Christian Schlötterer for providing the raw microsatellite data. V.Z. and S.V. collected the populations in Spain. V.Z. analyzed the population data and performed the neutrality tests, phylogenetic analyses, and microsatellite study. E.T. collected the populations in the UK and Sweden, advised and helped with the phylogenetic analyses and the bottleneck simulation, and provided the new European populations. C.P.K. and R.C. conceived the study, R.C. initially maintained the Spanish populations, C.P.K. supervised the study, and C.P.K. and V.Z. wrote the manuscript.

Publisher Copyright:
© 2017, © 2017 The Author(s).

Keywords

  • Drosophila melanogaster
  • Europe
  • cline
  • directional selection
  • timeless

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

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