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Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait.

Shirai LT, Saenko SV, Keller RA, Jerónimo MA, Brakefield PM, Descimon H, Wahlberg N, Beldade P - BMC Evol. Biol. (2012)

Bottom Line: We found variation between families, between subfamilies, and between tribes.The diversity in the combinations of genes expressed in association with eyespot formation does not parallel diversity in characteristics of the adult phenotype.We discuss these results in the context of inferring homology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, P-2780-156 Oeiras, Portugal.

ABSTRACT

Background: The origin and modification of novel traits are important aspects of biological diversification. Studies combining concepts and approaches of developmental genetics and evolutionary biology have uncovered many examples of the recruitment, or co-option, of genes conserved across lineages for the formation of novel, lineage-restricted traits. However, little is known about the evolutionary history of the recruitment of those genes, and of the relationship between them -for example, whether the co-option involves whole or parts of existing networks, or whether it occurs by redeployment of individual genes with de novo rewiring. We use a model novel trait, color pattern elements on butterfly wings called eyespots, to explore these questions. Eyespots have greatly diversified under natural and sexual selection, and their formation involves genetic circuitries shared across insects.

Results: We investigated the evolutionary history of the recruitment and co-recruitment of four conserved transcription regulators to the larval wing disc region where circular pattern elements develop. The co-localization of Antennapedia, Notch, Distal-less, and Spalt with presumptive (eye)spot organizers was examined in 13 butterfly species, providing the largest comparative dataset available for the system. We found variation between families, between subfamilies, and between tribes. Phylogenetic reconstructions by parsimony and maximum likelihood methods revealed an unambiguous evolutionary history only for Antennapedia, with a resolved single origin of eyespot-associated expression, and many homoplastic events for Notch, Distal-less, and Spalt. The flexibility in the (co-)recruitment of the targeted genes includes cases where different gene combinations are associated with morphologically similar eyespots, as well as cases where identical protein combinations are associated with very different phenotypes.

Conclusions: The evolutionary history of gene (co-)recruitment is consistent with both divergence from a recruited putative ancestral network, and with independent co-option of individual genes. The diversity in the combinations of genes expressed in association with eyespot formation does not parallel diversity in characteristics of the adult phenotype. We discuss these results in the context of inferring homology. Our study underscores the importance of widening the representation of phylogenetic, morphological, and genetic diversity in order to establish general principles about the mechanisms behind the evolution of novel traits.

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Localization of four developmental proteins in presumptive (eye)spots of outgroup species. Detection of Antp (green), N (yellow), Dll (red), and Sal (blue) proteins for outgroup species D. plexippus (Nymphalidae, Danainae), P. rapae (Pieridae), and P. machaon and P. apollo (Papilionidae) with the adult wing (left) and sample size (bottom right corner). J. coenia (Nymphalinae) and B. anynana (Satyrinae) expression patterns are shown as reference for respective subfamilies (cf. [9] and Figure 1). Note that, in some images, the localization of the eyespot organizer genes at the center of a wing compartment bordered by veins in larval wings does not associate to any eyespot in the adult wings. In these instances, the expression of such genes disappears during eyespot development but it reflects the potential of those compartments to form an eyespot (as it happens in some genetic stocks; see [36,38]).
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Figure 2: Localization of four developmental proteins in presumptive (eye)spots of outgroup species. Detection of Antp (green), N (yellow), Dll (red), and Sal (blue) proteins for outgroup species D. plexippus (Nymphalidae, Danainae), P. rapae (Pieridae), and P. machaon and P. apollo (Papilionidae) with the adult wing (left) and sample size (bottom right corner). J. coenia (Nymphalinae) and B. anynana (Satyrinae) expression patterns are shown as reference for respective subfamilies (cf. [9] and Figure 1). Note that, in some images, the localization of the eyespot organizer genes at the center of a wing compartment bordered by veins in larval wings does not associate to any eyespot in the adult wings. In these instances, the expression of such genes disappears during eyespot development but it reflects the potential of those compartments to form an eyespot (as it happens in some genetic stocks; see [36,38]).

Mentions: To investigate the evolutionary history of the co-option of conserved genes to the location of a developing novel trait, we analyzed expression patterns in larval wings of multiple species in different butterfly families. We targeted four genes involved in transcription regulation: transcription factors Antp, Dll, and Sal, and the transmembrane receptor N. The latter, when bound to its ligands (Delta/Serrate/LAG-2 family of proteins), releases an Intracellular domain that regulates gene expression when associated to DNA-binding CSL proteins [35]. The expression patterns of Antp, N, and Dll were previously analyzed across all stages of last-instar larval wings in nymphalids of subfamilies Nymphalinae and Satyrinae [9]. In this study, we added the expression analysis of Sal for those same species (Figure 1), and extended the phylogenetic sampling for all four genes to an outgroup comprised of another nymphalid subfamily (Danainae) and two other butterfly families (Pieridae and Papilionidae; Figure 2). Based on the complete dataset for all four proteins in the 13 representative species (Figure 3), we investigated the evolutionary history of the recruitment of these genes. We mapped the localization of transcription regulators in presumptive eyespot centers onto the species tree, and performed ancestral character reconstructions using both parsimony and maximum likelihood (ML) methods (Figure 4). The species chosen in this study represent diversity in (eye)spot morphology and position on the wing (cf. the conserved venation pattern), allowing for discussions about the inference of homology (Figure 5).


Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait.

Shirai LT, Saenko SV, Keller RA, Jerónimo MA, Brakefield PM, Descimon H, Wahlberg N, Beldade P - BMC Evol. Biol. (2012)

Localization of four developmental proteins in presumptive (eye)spots of outgroup species. Detection of Antp (green), N (yellow), Dll (red), and Sal (blue) proteins for outgroup species D. plexippus (Nymphalidae, Danainae), P. rapae (Pieridae), and P. machaon and P. apollo (Papilionidae) with the adult wing (left) and sample size (bottom right corner). J. coenia (Nymphalinae) and B. anynana (Satyrinae) expression patterns are shown as reference for respective subfamilies (cf. [9] and Figure 1). Note that, in some images, the localization of the eyespot organizer genes at the center of a wing compartment bordered by veins in larval wings does not associate to any eyespot in the adult wings. In these instances, the expression of such genes disappears during eyespot development but it reflects the potential of those compartments to form an eyespot (as it happens in some genetic stocks; see [36,38]).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3361465&req=5

Figure 2: Localization of four developmental proteins in presumptive (eye)spots of outgroup species. Detection of Antp (green), N (yellow), Dll (red), and Sal (blue) proteins for outgroup species D. plexippus (Nymphalidae, Danainae), P. rapae (Pieridae), and P. machaon and P. apollo (Papilionidae) with the adult wing (left) and sample size (bottom right corner). J. coenia (Nymphalinae) and B. anynana (Satyrinae) expression patterns are shown as reference for respective subfamilies (cf. [9] and Figure 1). Note that, in some images, the localization of the eyespot organizer genes at the center of a wing compartment bordered by veins in larval wings does not associate to any eyespot in the adult wings. In these instances, the expression of such genes disappears during eyespot development but it reflects the potential of those compartments to form an eyespot (as it happens in some genetic stocks; see [36,38]).
Mentions: To investigate the evolutionary history of the co-option of conserved genes to the location of a developing novel trait, we analyzed expression patterns in larval wings of multiple species in different butterfly families. We targeted four genes involved in transcription regulation: transcription factors Antp, Dll, and Sal, and the transmembrane receptor N. The latter, when bound to its ligands (Delta/Serrate/LAG-2 family of proteins), releases an Intracellular domain that regulates gene expression when associated to DNA-binding CSL proteins [35]. The expression patterns of Antp, N, and Dll were previously analyzed across all stages of last-instar larval wings in nymphalids of subfamilies Nymphalinae and Satyrinae [9]. In this study, we added the expression analysis of Sal for those same species (Figure 1), and extended the phylogenetic sampling for all four genes to an outgroup comprised of another nymphalid subfamily (Danainae) and two other butterfly families (Pieridae and Papilionidae; Figure 2). Based on the complete dataset for all four proteins in the 13 representative species (Figure 3), we investigated the evolutionary history of the recruitment of these genes. We mapped the localization of transcription regulators in presumptive eyespot centers onto the species tree, and performed ancestral character reconstructions using both parsimony and maximum likelihood (ML) methods (Figure 4). The species chosen in this study represent diversity in (eye)spot morphology and position on the wing (cf. the conserved venation pattern), allowing for discussions about the inference of homology (Figure 5).

Bottom Line: We found variation between families, between subfamilies, and between tribes.The diversity in the combinations of genes expressed in association with eyespot formation does not parallel diversity in characteristics of the adult phenotype.We discuss these results in the context of inferring homology.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, P-2780-156 Oeiras, Portugal.

ABSTRACT

Background: The origin and modification of novel traits are important aspects of biological diversification. Studies combining concepts and approaches of developmental genetics and evolutionary biology have uncovered many examples of the recruitment, or co-option, of genes conserved across lineages for the formation of novel, lineage-restricted traits. However, little is known about the evolutionary history of the recruitment of those genes, and of the relationship between them -for example, whether the co-option involves whole or parts of existing networks, or whether it occurs by redeployment of individual genes with de novo rewiring. We use a model novel trait, color pattern elements on butterfly wings called eyespots, to explore these questions. Eyespots have greatly diversified under natural and sexual selection, and their formation involves genetic circuitries shared across insects.

Results: We investigated the evolutionary history of the recruitment and co-recruitment of four conserved transcription regulators to the larval wing disc region where circular pattern elements develop. The co-localization of Antennapedia, Notch, Distal-less, and Spalt with presumptive (eye)spot organizers was examined in 13 butterfly species, providing the largest comparative dataset available for the system. We found variation between families, between subfamilies, and between tribes. Phylogenetic reconstructions by parsimony and maximum likelihood methods revealed an unambiguous evolutionary history only for Antennapedia, with a resolved single origin of eyespot-associated expression, and many homoplastic events for Notch, Distal-less, and Spalt. The flexibility in the (co-)recruitment of the targeted genes includes cases where different gene combinations are associated with morphologically similar eyespots, as well as cases where identical protein combinations are associated with very different phenotypes.

Conclusions: The evolutionary history of gene (co-)recruitment is consistent with both divergence from a recruited putative ancestral network, and with independent co-option of individual genes. The diversity in the combinations of genes expressed in association with eyespot formation does not parallel diversity in characteristics of the adult phenotype. We discuss these results in the context of inferring homology. Our study underscores the importance of widening the representation of phylogenetic, morphological, and genetic diversity in order to establish general principles about the mechanisms behind the evolution of novel traits.

Show MeSH