TY - JOUR
T1 - Evolutionary coincidence of adaptive changes in exuperantia and the emergence of bicoid in Cyclorrhapha (Diptera)
AU - de Oliveira, Janaina Lima
AU - Sobrinho-Junior, Iderval Silva
AU - Chahad-Ehlers, Samira
AU - de Brito, Reinaldo Alves
PY - 2017/9/1
Y1 - 2017/9/1
N2 - The great radiation in the infraorder Cyclorrhapha involved several morphological and molecular changes, including important changes in anterior egg development. During Drosophila oogenesis, exuperantia (exu) is critical for localizing bicoid (bcd) messenger RNA (mRNA) to the anterior region of the oocyte. Because it is phylogenetically older than bcd, which is exclusive to Cyclorrhapha, we hypothesize that exu has undergone adaptive changes to enable this new function. Although exu has been well studied in Drosophila, there is no functional or transcriptional information about it in any other Diptera. Here, we investigate exu in the South American fruit fly Anastrepha fraterculus, a Cyclorrhapha of great agricultural importance that have lost bcd, aiming to understand the evolution of exu in this infraorder. We assessed its pattern of gene expression in A. fraterculus by analyzing transcriptomes from cephalic and reproductive tissues. A combination of next-generation data with classical sequencing procedures enabled identification of the structure of exu and its alternative transcripts in this species. In addition to the sex-specific isoforms described for Drosophila, we found that not only exu is expressed in heads, but this is mediated by two transcripts with a specific 5′UTR exon—likely a result from usage of a third promoter. Furthermore, we tested the hypothesis that exu is evolving under positive selection in Cyclorrhapha after divergence from lower Diptera. We found evidence of positive selection at two important exu domains, EXO-like and SAM-like, both involved with mRNA binding during bcd mRNA localization in Drosophila, which could reflect its cooptation for the new function of bcd mRNA localization in Cyclorrhapha.
AB - The great radiation in the infraorder Cyclorrhapha involved several morphological and molecular changes, including important changes in anterior egg development. During Drosophila oogenesis, exuperantia (exu) is critical for localizing bicoid (bcd) messenger RNA (mRNA) to the anterior region of the oocyte. Because it is phylogenetically older than bcd, which is exclusive to Cyclorrhapha, we hypothesize that exu has undergone adaptive changes to enable this new function. Although exu has been well studied in Drosophila, there is no functional or transcriptional information about it in any other Diptera. Here, we investigate exu in the South American fruit fly Anastrepha fraterculus, a Cyclorrhapha of great agricultural importance that have lost bcd, aiming to understand the evolution of exu in this infraorder. We assessed its pattern of gene expression in A. fraterculus by analyzing transcriptomes from cephalic and reproductive tissues. A combination of next-generation data with classical sequencing procedures enabled identification of the structure of exu and its alternative transcripts in this species. In addition to the sex-specific isoforms described for Drosophila, we found that not only exu is expressed in heads, but this is mediated by two transcripts with a specific 5′UTR exon—likely a result from usage of a third promoter. Furthermore, we tested the hypothesis that exu is evolving under positive selection in Cyclorrhapha after divergence from lower Diptera. We found evidence of positive selection at two important exu domains, EXO-like and SAM-like, both involved with mRNA binding during bcd mRNA localization in Drosophila, which could reflect its cooptation for the new function of bcd mRNA localization in Cyclorrhapha.
KW - Anastrepha
KW - Bicoid
KW - Cooptation
KW - Cyclorrhapha
KW - Exuperantia
KW - Positive selection
UR - http://www.scopus.com/inward/record.url?scp=85029072588&partnerID=8YFLogxK
UR - http://dx.doi.org/10.1007/s00427-017-0594-3
U2 - 10.1007/s00427-017-0594-3
DO - 10.1007/s00427-017-0594-3
M3 - Article
AN - SCOPUS:85029072588
SN - 0949-944X
VL - 227
SP - 355
EP - 365
JO - Development Genes and Evolution
JF - Development Genes and Evolution
IS - 5
ER -