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Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

Chen S, Armistead JS, Provost-Javier KN, Sakamoto JM, Rasgon JL - BMC Evol. Biol. (2010)

Bottom Line: In Aedes, smaller fragments have undergone gene conversion events.The study shows concerted evolution and purifying selection shaped the evolution of mosquito Vtg genes following gene duplication.Additionally, similar evolutionary patterns were observed in the Vtg genes from other invertebrate and vertebrate organisms, suggesting that duplication, concerted evolution and purifying selection may be the major evolutionary forces driving Vtg gene evolution across highly divergent taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA.

ABSTRACT

Background: Mosquito vitellogenin (Vtg) genes belong to a small multiple gene family that encodes the major yolk protein precursors required for egg production. Multiple Vtg genes have been cloned and characterized from several mosquito species, but their origin and molecular evolution are poorly understood.

Results: Here we used in silico and molecular cloning techniques to identify and characterize the evolution of the Vtg gene family from the genera Culex, Aedes/Ochlerotatus, and Anopheles. We identified the probable ancestral Vtg gene among different mosquito species by its conserved association with a novel gene approximately one kilobase upstream of the start codon. Phylogenetic analysis indicated that the Vtg gene family arose by duplication events, but that the pattern of duplication was different in each mosquito genera. Signatures of purifying selection were detected in Culex, Aedes and Anopheles. Gene conversion is a major driver of concerted evolution in Culex, while unequal crossover is likely the major driver of concerted evolution in Anopheles. In Aedes, smaller fragments have undergone gene conversion events.

Conclusions: The study shows concerted evolution and purifying selection shaped the evolution of mosquito Vtg genes following gene duplication. Additionally, similar evolutionary patterns were observed in the Vtg genes from other invertebrate and vertebrate organisms, suggesting that duplication, concerted evolution and purifying selection may be the major evolutionary forces driving Vtg gene evolution across highly divergent taxa.

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Phylogenetic analysis of mosquito Vtg genes. Phylogenetic analysis of mosquito vitellogenin gene sequences was conducted using Maximum Likelihood, Bayesian and Neighbor-joining methods; numbers at nodes indicate support values for each method (in that order). T37L-associated (putative ancestral) Vtg copies in different mosquito species are indicated by "*". Vtg gene of honey bee Apis mellifera (accession number AJ517411) was used as outgroup. Vtg gene accession numbers are AJ517411 for honey bee, AY691327 for AaVgC and the remainder are listed in Table 2.
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Figure 4: Phylogenetic analysis of mosquito Vtg genes. Phylogenetic analysis of mosquito vitellogenin gene sequences was conducted using Maximum Likelihood, Bayesian and Neighbor-joining methods; numbers at nodes indicate support values for each method (in that order). T37L-associated (putative ancestral) Vtg copies in different mosquito species are indicated by "*". Vtg gene of honey bee Apis mellifera (accession number AJ517411) was used as outgroup. Vtg gene accession numbers are AJ517411 for honey bee, AY691327 for AaVgC and the remainder are listed in Table 2.

Mentions: Phylogenetic analysis using the full Vtg coding sequences was used to examine the evolution of Vtg genes among mosquitoes (Figure 4). All analyses gave identical tree morphology. With the exception of the Culex Vg2 group (which represents a duplication event unique to the genus Culex), all other mosquito Vtg genes conformed to three major clades: Aedes/Ochlerotatus, Culex and Anopheles. The Aedes/Ochlerotatus clade is more closely related to the Culex Vg1 clade than the Anopheles clade, which is in agreement with the agreed relationships of these genera. Paralogous copies cluster more closely than orthologues within each clade. Three independent duplication patterns were observed among mosquito genera. In Culex, a divergent duplication event produced the Vg1 and Vg2 genes, which each then underwent additional independent duplications generating four Vtg genes in total. These duplication events occurred prior to the divergence of pipiens and tarsalis within the genus. The absence of Vg2 homologues in non-Culex genera may reflect a unique duplication event in Culex, or less likely, independent gene loss events in Anopheles and Aedes/Ochlerotatus. In Aedes, the early duplication from the ancestral copy generated the VgA/B lineage, which underwent an additional duplication to generate 3 Vtg copies - these duplication events occurred prior to the divergence of the Aedes and Ochlerotatus genera. In Anopheles, Vtg gene duplication events occurred rapidly during tandem repeat generation (Figure 4). Unlike Culex and Aedes/Ochlerotatus, none of the An. gambiae Vtg genes cluster with other members of the genus, suggesting that the rapid tandem repeat generation occurred after the split of gambiae from the other members of the Anopheles genus.


Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

Chen S, Armistead JS, Provost-Javier KN, Sakamoto JM, Rasgon JL - BMC Evol. Biol. (2010)

Phylogenetic analysis of mosquito Vtg genes. Phylogenetic analysis of mosquito vitellogenin gene sequences was conducted using Maximum Likelihood, Bayesian and Neighbor-joining methods; numbers at nodes indicate support values for each method (in that order). T37L-associated (putative ancestral) Vtg copies in different mosquito species are indicated by "*". Vtg gene of honey bee Apis mellifera (accession number AJ517411) was used as outgroup. Vtg gene accession numbers are AJ517411 for honey bee, AY691327 for AaVgC and the remainder are listed in Table 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2875236&req=5

Figure 4: Phylogenetic analysis of mosquito Vtg genes. Phylogenetic analysis of mosquito vitellogenin gene sequences was conducted using Maximum Likelihood, Bayesian and Neighbor-joining methods; numbers at nodes indicate support values for each method (in that order). T37L-associated (putative ancestral) Vtg copies in different mosquito species are indicated by "*". Vtg gene of honey bee Apis mellifera (accession number AJ517411) was used as outgroup. Vtg gene accession numbers are AJ517411 for honey bee, AY691327 for AaVgC and the remainder are listed in Table 2.
Mentions: Phylogenetic analysis using the full Vtg coding sequences was used to examine the evolution of Vtg genes among mosquitoes (Figure 4). All analyses gave identical tree morphology. With the exception of the Culex Vg2 group (which represents a duplication event unique to the genus Culex), all other mosquito Vtg genes conformed to three major clades: Aedes/Ochlerotatus, Culex and Anopheles. The Aedes/Ochlerotatus clade is more closely related to the Culex Vg1 clade than the Anopheles clade, which is in agreement with the agreed relationships of these genera. Paralogous copies cluster more closely than orthologues within each clade. Three independent duplication patterns were observed among mosquito genera. In Culex, a divergent duplication event produced the Vg1 and Vg2 genes, which each then underwent additional independent duplications generating four Vtg genes in total. These duplication events occurred prior to the divergence of pipiens and tarsalis within the genus. The absence of Vg2 homologues in non-Culex genera may reflect a unique duplication event in Culex, or less likely, independent gene loss events in Anopheles and Aedes/Ochlerotatus. In Aedes, the early duplication from the ancestral copy generated the VgA/B lineage, which underwent an additional duplication to generate 3 Vtg copies - these duplication events occurred prior to the divergence of the Aedes and Ochlerotatus genera. In Anopheles, Vtg gene duplication events occurred rapidly during tandem repeat generation (Figure 4). Unlike Culex and Aedes/Ochlerotatus, none of the An. gambiae Vtg genes cluster with other members of the genus, suggesting that the rapid tandem repeat generation occurred after the split of gambiae from the other members of the Anopheles genus.

Bottom Line: In Aedes, smaller fragments have undergone gene conversion events.The study shows concerted evolution and purifying selection shaped the evolution of mosquito Vtg genes following gene duplication.Additionally, similar evolutionary patterns were observed in the Vtg genes from other invertebrate and vertebrate organisms, suggesting that duplication, concerted evolution and purifying selection may be the major evolutionary forces driving Vtg gene evolution across highly divergent taxa.

View Article: PubMed Central - HTML - PubMed

Affiliation: The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA.

ABSTRACT

Background: Mosquito vitellogenin (Vtg) genes belong to a small multiple gene family that encodes the major yolk protein precursors required for egg production. Multiple Vtg genes have been cloned and characterized from several mosquito species, but their origin and molecular evolution are poorly understood.

Results: Here we used in silico and molecular cloning techniques to identify and characterize the evolution of the Vtg gene family from the genera Culex, Aedes/Ochlerotatus, and Anopheles. We identified the probable ancestral Vtg gene among different mosquito species by its conserved association with a novel gene approximately one kilobase upstream of the start codon. Phylogenetic analysis indicated that the Vtg gene family arose by duplication events, but that the pattern of duplication was different in each mosquito genera. Signatures of purifying selection were detected in Culex, Aedes and Anopheles. Gene conversion is a major driver of concerted evolution in Culex, while unequal crossover is likely the major driver of concerted evolution in Anopheles. In Aedes, smaller fragments have undergone gene conversion events.

Conclusions: The study shows concerted evolution and purifying selection shaped the evolution of mosquito Vtg genes following gene duplication. Additionally, similar evolutionary patterns were observed in the Vtg genes from other invertebrate and vertebrate organisms, suggesting that duplication, concerted evolution and purifying selection may be the major evolutionary forces driving Vtg gene evolution across highly divergent taxa.

Show MeSH