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Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait.

Saenko SV, Marialva MS, Beldade P - Evodevo (2011)

Bottom Line: Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns.Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots.Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands. pbeldade@igc.gulbenkian.pt.

ABSTRACT

Background: Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns. Changes in embryonic expression and activity of Hox genes were crucial in the evolution of animal body plans, but their role in the post-embryonic development of lineage-specific traits remains largely unexplored. Here, we focus on the insect Hox genes Ultrabithorax (Ubx) and Antennapedia (Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns.

Results: First, we describe a conserved pattern of Ubx expression and a novel pattern of Antp expression in wing discs of Bicyclus anynana butterflies. The discrete, reiterated domains of Antp contrast with the typical expression of Hox genes in single continuous regions in arthropod embryos. Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots. Antp upregulation is the earliest event in organizer development described to date, and in contrast to all genes implicated in eyespot formation, is exclusive to those centres. Third, our comparative analysis of gene expression across nymphalids reveals unexpected differences in organizer determination.

Conclusions: We show that the Antp's recruitment for the formation of novel traits in butterfly wing discs involved the evolution of new expression domains, and is restricted to a particular lineage. This study contributes novel insights into the evolution of Antp expression, as well as into the genetic mechanisms underlying morphological diversification. Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

No MeSH data available.


Related in: MedlinePlus

Genetic divergence in determination of nymphalid eyespot organizers. (A) Localization of Antp (green), N (yellow) and Dll (red) in larval wing discs of representatives of the subfamily Satyrinae. Shown are sections of adult wings and the corresponding sections of larval wing discs at late stages of development, when tracheae are extended into vein lacunae (visible here as black lines). N and Dll are initially expressed in non-organizer areas (both in the intervein stripes, and Dll also along the wing margin), their expression in eyespot organizing centres occurs after extension of the trachea into the lacunae (except in the basal satyrine C. memnon). (B) Expression of N and Dll in subfamily Nymphalinae resembles that in Satyrinae, but Antp is absent from eyespot organizers at all stages of larval wing development. In both panels, numbers of individuals used for gene expression analysis in larval wings are shown on adult wing image. (C) Phylogenetic relationship among butterflies examined in this study, following [45].
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Figure 2: Genetic divergence in determination of nymphalid eyespot organizers. (A) Localization of Antp (green), N (yellow) and Dll (red) in larval wing discs of representatives of the subfamily Satyrinae. Shown are sections of adult wings and the corresponding sections of larval wing discs at late stages of development, when tracheae are extended into vein lacunae (visible here as black lines). N and Dll are initially expressed in non-organizer areas (both in the intervein stripes, and Dll also along the wing margin), their expression in eyespot organizing centres occurs after extension of the trachea into the lacunae (except in the basal satyrine C. memnon). (B) Expression of N and Dll in subfamily Nymphalinae resembles that in Satyrinae, but Antp is absent from eyespot organizers at all stages of larval wing development. In both panels, numbers of individuals used for gene expression analysis in larval wings are shown on adult wing image. (C) Phylogenetic relationship among butterflies examined in this study, following [45].

Mentions: Our analysis of Antp expression in B. anynana (subfamily Satyrinae) suggested a role in the establishment of eyespot organizers. Next, we investigated whether this Hox gene plays a similar role in another nymphalid eyespot model, Junonia coenia (subfamily Nymphalinae). Despite the fact that the two species have diverged some 90 MYA [45], their eyespots have strikingly similar appearance: in both species they are formed by a central white pupil, an inner black disc, and an outer golden ring (Figure 2). Like all nymphalid border ocelli, they are thought to have a common evolutionary origin [21]. Surprisingly, our analysis of wing discs from 85 J. coenia individuals, covering all stages of the last instar wing development, revealed that, in contrast to what happens in B. anynana (Figure 2A), Antp is never expressed in eyespot organizers or elsewhere in the wings of J. coenia (Figure 2B). Immunostainings in embryos of B. anynana and J. coenia (Figure 1E) showed typical expression of Antp (strong in the thorax and weak in the abdomen [46-48]), confirming that the anti-Antp antibody does recognize the target protein in both species. In contrast to Antp, N and Dll were detected in the intervein midlines and in eyespot organizers in both lab models (Figure 2A, B). These findings suggest that expression of N and Dll in J. coenia is under the control of some other factors, and that the regulatory network establishing eyespot organizing centres is not as conserved as previously thought [26]. We, therefore, examined whether other genes, implicated in eyespot formation in J. coenia, and assumed to play similar roles in B. anynana, have comparable expression patterns in both species.


Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait.

Saenko SV, Marialva MS, Beldade P - Evodevo (2011)

Genetic divergence in determination of nymphalid eyespot organizers. (A) Localization of Antp (green), N (yellow) and Dll (red) in larval wing discs of representatives of the subfamily Satyrinae. Shown are sections of adult wings and the corresponding sections of larval wing discs at late stages of development, when tracheae are extended into vein lacunae (visible here as black lines). N and Dll are initially expressed in non-organizer areas (both in the intervein stripes, and Dll also along the wing margin), their expression in eyespot organizing centres occurs after extension of the trachea into the lacunae (except in the basal satyrine C. memnon). (B) Expression of N and Dll in subfamily Nymphalinae resembles that in Satyrinae, but Antp is absent from eyespot organizers at all stages of larval wing development. In both panels, numbers of individuals used for gene expression analysis in larval wings are shown on adult wing image. (C) Phylogenetic relationship among butterflies examined in this study, following [45].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3108338&req=5

Figure 2: Genetic divergence in determination of nymphalid eyespot organizers. (A) Localization of Antp (green), N (yellow) and Dll (red) in larval wing discs of representatives of the subfamily Satyrinae. Shown are sections of adult wings and the corresponding sections of larval wing discs at late stages of development, when tracheae are extended into vein lacunae (visible here as black lines). N and Dll are initially expressed in non-organizer areas (both in the intervein stripes, and Dll also along the wing margin), their expression in eyespot organizing centres occurs after extension of the trachea into the lacunae (except in the basal satyrine C. memnon). (B) Expression of N and Dll in subfamily Nymphalinae resembles that in Satyrinae, but Antp is absent from eyespot organizers at all stages of larval wing development. In both panels, numbers of individuals used for gene expression analysis in larval wings are shown on adult wing image. (C) Phylogenetic relationship among butterflies examined in this study, following [45].
Mentions: Our analysis of Antp expression in B. anynana (subfamily Satyrinae) suggested a role in the establishment of eyespot organizers. Next, we investigated whether this Hox gene plays a similar role in another nymphalid eyespot model, Junonia coenia (subfamily Nymphalinae). Despite the fact that the two species have diverged some 90 MYA [45], their eyespots have strikingly similar appearance: in both species they are formed by a central white pupil, an inner black disc, and an outer golden ring (Figure 2). Like all nymphalid border ocelli, they are thought to have a common evolutionary origin [21]. Surprisingly, our analysis of wing discs from 85 J. coenia individuals, covering all stages of the last instar wing development, revealed that, in contrast to what happens in B. anynana (Figure 2A), Antp is never expressed in eyespot organizers or elsewhere in the wings of J. coenia (Figure 2B). Immunostainings in embryos of B. anynana and J. coenia (Figure 1E) showed typical expression of Antp (strong in the thorax and weak in the abdomen [46-48]), confirming that the anti-Antp antibody does recognize the target protein in both species. In contrast to Antp, N and Dll were detected in the intervein midlines and in eyespot organizers in both lab models (Figure 2A, B). These findings suggest that expression of N and Dll in J. coenia is under the control of some other factors, and that the regulatory network establishing eyespot organizing centres is not as conserved as previously thought [26]. We, therefore, examined whether other genes, implicated in eyespot formation in J. coenia, and assumed to play similar roles in B. anynana, have comparable expression patterns in both species.

Bottom Line: Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns.Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots.Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands. pbeldade@igc.gulbenkian.pt.

ABSTRACT

Background: Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns. Changes in embryonic expression and activity of Hox genes were crucial in the evolution of animal body plans, but their role in the post-embryonic development of lineage-specific traits remains largely unexplored. Here, we focus on the insect Hox genes Ultrabithorax (Ubx) and Antennapedia (Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns.

Results: First, we describe a conserved pattern of Ubx expression and a novel pattern of Antp expression in wing discs of Bicyclus anynana butterflies. The discrete, reiterated domains of Antp contrast with the typical expression of Hox genes in single continuous regions in arthropod embryos. Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots. Antp upregulation is the earliest event in organizer development described to date, and in contrast to all genes implicated in eyespot formation, is exclusive to those centres. Third, our comparative analysis of gene expression across nymphalids reveals unexpected differences in organizer determination.

Conclusions: We show that the Antp's recruitment for the formation of novel traits in butterfly wing discs involved the evolution of new expression domains, and is restricted to a particular lineage. This study contributes novel insights into the evolution of Antp expression, as well as into the genetic mechanisms underlying morphological diversification. Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

No MeSH data available.


Related in: MedlinePlus