Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction

J. MENSCH; N. LAVAGNINO; V. CARREIRA; A. MASSALDI; E. HASSON; J. J. FANARA

BMC DEVELOPMENTAL BIOLOGY

BioMed Central Ltd

Año: 2008 p. 78 - 89

1471-213X

Background Understanding  the genetic architecture of ecologically  relevant adaptive  traits requires  the contribution  of  developmental  and  evolutionary  biology.  The  time  to  reach  the  age  of reproduction  is  a  complex  life  history  trait  commonly  known  as  developmental  time.  In particular,  in  holometabolous  insects  that  occupy  ephemeral  habitats,  like  fruit  flies,  the impact of developmental time on fitness is further exaggerated. The present work is one of the  first  systematic  studies  of  the  genetic  basis  of  developmental  time,  in which we  also evaluate the impact of environmental variation on the expression of the trait. Results We  analyzed  179  co-isogenic  single  P[GT1]-element  insertion  lines  of  Drosophila melanogaster  to  identify novel genes affecting developmental  time  in flies reared at 25ºC. Sixty  percent  of  the  lines  showed  a  heterochronic  phenotype,  suggesting  that  a  large number of genes affect  this  trait. Mutant  lines  for  the genes Merlin and Karl  showed  the most  extreme  phenotypes  exhibiting  a  developmental  time  reduction  and  increase, respectively,  of  over  2  days  and  4  days  relative  to  the  control  (a  co-isogenic  P-element insertion free  line). In addition, a subset of 42  lines selected at random from  the  initial set of  179  lines  was  screened  at  17ºC.  Interestingly,  the  gene-by-environment  interaction accounted  for 52% of  total phenotypic variance. Plastic  reaction norms were  found  for  a large number of developmental time candidate genes. Conclusions We identified components of several integrated time-dependent pathways affecting egg-to-adult  developmental  time  in  Drosophila.  At  the  same  time,  we  also  show  that  many heterochronic  phenotypes  may  arise  from  changes  in  genes  involved  in  several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate  that many developmental  time genes have pleiotropic effects on  several adult  traits  and  that  the  action  of  most  of  them  is  sensitive  to  temperature  during development. Taken  together, our results stress  the need  to  take  into account  the effect of environmental variation and  the dynamics of gene  interactions on  the genetic architecture of this complex life-history trait.