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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

Gene expression in the eyespot model Bicyclus anynana (Nymphalidae, Satyrinae). (A) Fore-(top) and hindwing (bottom) of 'wild-type' adult and larval wing discs visualized for Ubx (blue) and Antp (green). Ubx is detected throughout the hindwing, but not in the forewing (as is characteristic of insects), and is not associated with any colour pattern element (the bright spot visible in the forewing is an artefact). Antp is detected in the presumptive eyespot organizers in both fore- and hindwing. (B) Adult (top) and larval (bottom) hindwing of Cyclops venation mutant with altered eyespot number and shape [28]: Antp is upregulated in a single elongated organizer, matching the morphology of the adult eyespot centre. (C) Larval hindwings stained for Antp mRNA (left) and protein (right). Antp is detected in eyespot centres shortly after the last larval molt, prior to the extension of trachea into the vein lacunae (arrows) and before the upregulation of other organizer proteins (co-stainings of Antp, N and Dll in early wings are shown in Additional File 1). (D) Larval hindwings stained for hh and ptc mRNA. Absence of both transcripts in B. anynana eyespot fields (in contrast to J. coenia [33]) reveals genetic divergence in organizer determination. (E) Immunostainings in embryos of B. anynana (left) and J. coenia (right) at 30 to 40% development [63] show the typical pattern of Antp in thorax and abdomen. Proteins are shown in colours, mRNA in gray; numbers indicate individuals examined.
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Figure 1: Gene expression in the eyespot model Bicyclus anynana (Nymphalidae, Satyrinae). (A) Fore-(top) and hindwing (bottom) of 'wild-type' adult and larval wing discs visualized for Ubx (blue) and Antp (green). Ubx is detected throughout the hindwing, but not in the forewing (as is characteristic of insects), and is not associated with any colour pattern element (the bright spot visible in the forewing is an artefact). Antp is detected in the presumptive eyespot organizers in both fore- and hindwing. (B) Adult (top) and larval (bottom) hindwing of Cyclops venation mutant with altered eyespot number and shape [28]: Antp is upregulated in a single elongated organizer, matching the morphology of the adult eyespot centre. (C) Larval hindwings stained for Antp mRNA (left) and protein (right). Antp is detected in eyespot centres shortly after the last larval molt, prior to the extension of trachea into the vein lacunae (arrows) and before the upregulation of other organizer proteins (co-stainings of Antp, N and Dll in early wings are shown in Additional File 1). (D) Larval hindwings stained for hh and ptc mRNA. Absence of both transcripts in B. anynana eyespot fields (in contrast to J. coenia [33]) reveals genetic divergence in organizer determination. (E) Immunostainings in embryos of B. anynana (left) and J. coenia (right) at 30 to 40% development [63] show the typical pattern of Antp in thorax and abdomen. Proteins are shown in colours, mRNA in gray; numbers indicate individuals examined.

Mentions: Immunostainings in larval wing discs of Bicyclus anynana revealed a conserved expression pattern for Ubx and a novel expression pattern for Antp. In 30 individuals examined, spanning all sequential stages of larval wing development (cf. the extent of tracheal extension into vein lacunae [35]), the Ubx protein was detected throughout the entire hindwing and nowhere in the forewing (Figure 1A). The difference between fore- and hindwing is identical to that described in other insects and is consistent with Ubx's role in the specification of the third thoracic segment, including the associated appendages and their characteristics [13-15]. The fact that Ubx is expressed ubiquitously on the hindwing with no association to any particular wing regions suggests that this Hox gene, for which changes in expression have been associated with colour pattern transformations in J. coenia [13], is not involved in the determination of any specific colour pattern element in B. anynana.


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

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

Gene expression in the eyespot model Bicyclus anynana (Nymphalidae, Satyrinae). (A) Fore-(top) and hindwing (bottom) of 'wild-type' adult and larval wing discs visualized for Ubx (blue) and Antp (green). Ubx is detected throughout the hindwing, but not in the forewing (as is characteristic of insects), and is not associated with any colour pattern element (the bright spot visible in the forewing is an artefact). Antp is detected in the presumptive eyespot organizers in both fore- and hindwing. (B) Adult (top) and larval (bottom) hindwing of Cyclops venation mutant with altered eyespot number and shape [28]: Antp is upregulated in a single elongated organizer, matching the morphology of the adult eyespot centre. (C) Larval hindwings stained for Antp mRNA (left) and protein (right). Antp is detected in eyespot centres shortly after the last larval molt, prior to the extension of trachea into the vein lacunae (arrows) and before the upregulation of other organizer proteins (co-stainings of Antp, N and Dll in early wings are shown in Additional File 1). (D) Larval hindwings stained for hh and ptc mRNA. Absence of both transcripts in B. anynana eyespot fields (in contrast to J. coenia [33]) reveals genetic divergence in organizer determination. (E) Immunostainings in embryos of B. anynana (left) and J. coenia (right) at 30 to 40% development [63] show the typical pattern of Antp in thorax and abdomen. Proteins are shown in colours, mRNA in gray; numbers indicate individuals examined.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Gene expression in the eyespot model Bicyclus anynana (Nymphalidae, Satyrinae). (A) Fore-(top) and hindwing (bottom) of 'wild-type' adult and larval wing discs visualized for Ubx (blue) and Antp (green). Ubx is detected throughout the hindwing, but not in the forewing (as is characteristic of insects), and is not associated with any colour pattern element (the bright spot visible in the forewing is an artefact). Antp is detected in the presumptive eyespot organizers in both fore- and hindwing. (B) Adult (top) and larval (bottom) hindwing of Cyclops venation mutant with altered eyespot number and shape [28]: Antp is upregulated in a single elongated organizer, matching the morphology of the adult eyespot centre. (C) Larval hindwings stained for Antp mRNA (left) and protein (right). Antp is detected in eyespot centres shortly after the last larval molt, prior to the extension of trachea into the vein lacunae (arrows) and before the upregulation of other organizer proteins (co-stainings of Antp, N and Dll in early wings are shown in Additional File 1). (D) Larval hindwings stained for hh and ptc mRNA. Absence of both transcripts in B. anynana eyespot fields (in contrast to J. coenia [33]) reveals genetic divergence in organizer determination. (E) Immunostainings in embryos of B. anynana (left) and J. coenia (right) at 30 to 40% development [63] show the typical pattern of Antp in thorax and abdomen. Proteins are shown in colours, mRNA in gray; numbers indicate individuals examined.
Mentions: Immunostainings in larval wing discs of Bicyclus anynana revealed a conserved expression pattern for Ubx and a novel expression pattern for Antp. In 30 individuals examined, spanning all sequential stages of larval wing development (cf. the extent of tracheal extension into vein lacunae [35]), the Ubx protein was detected throughout the entire hindwing and nowhere in the forewing (Figure 1A). The difference between fore- and hindwing is identical to that described in other insects and is consistent with Ubx's role in the specification of the third thoracic segment, including the associated appendages and their characteristics [13-15]. The fact that Ubx is expressed ubiquitously on the hindwing with no association to any particular wing regions suggests that this Hox gene, for which changes in expression have been associated with colour pattern transformations in J. coenia [13], is not involved in the determination of any specific colour pattern element in B. anynana.

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