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The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus.

Thompson MJ, Timmermans MJ, Jiggins CD, Vogler AP - BMC Evol. Biol. (2014)

Bottom Line: Gene trees for invected do not show this pattern.A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, Natural History Museum, London SW7 5BD, UK. martt@nhm.ac.uk.

ABSTRACT

Background: The phylogenetic history of genes underlying phenotypic diversity can offer insight into the evolutionary origin of adaptive traits. This is especially true where single genes have large phenotypic effects, for example in determining polymorphic mimicry in butterflies. Here, we characterise the evolutionary history of two candidate genes for the mimicry switch in the polymorphic Batesian mimic Papilio dardanus coding for the transcription factors engrailed and invected.

Results: We show that phased haplotypes associated with the dominant morphs f. poultoni and f. planemoides are phylogenetically highly divergent, in particular at non-synonymous sites. Some non-synonymous changes are shared between the divergent alleles suggesting either convergence or a shared ancestry. Gene trees for invected do not show this pattern. Despite their great divergence, all engrailed alleles of P. dardanus were monophyletic with respect to alleles of closely related species. Phylogenetic analyses therefore reveal no evidence for introgression from other species. A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.

Conclusions: The divergence between engrailed haplotypes suggests an evolutionary history distorted by selection with multiple changes reflecting recurrent selective sweeps. The high level of intraspecific polymorphism observed is characteristic of balancing selection on this locus, as expected if the gene engrailed is under phenotypic selection for the maintenance of multiple mimetic morphs. Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.

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The structure of genetic variation in invected and engrailed. Gene trees were established by maximum likelihood for invected (A) and engrailed (B) haplotypes, separately from non-synonymous and synonymous nucleotide changes. Branch lengths correspond to the number of changes. The area of each pie is scaled in proportion to the frequency of that haplotype among the morphs sampled, and colours of pies reflect proportion of haplotypes recovered from each morph, labelled as in Figure 4. (C) Unique SNPs in the two morph-associated alleles relative to the consensus sequence for all other inferred P. dardanus alleles.
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Fig7: The structure of genetic variation in invected and engrailed. Gene trees were established by maximum likelihood for invected (A) and engrailed (B) haplotypes, separately from non-synonymous and synonymous nucleotide changes. Branch lengths correspond to the number of changes. The area of each pie is scaled in proportion to the frequency of that haplotype among the morphs sampled, and colours of pies reflect proportion of haplotypes recovered from each morph, labelled as in Figure 4. (C) Unique SNPs in the two morph-associated alleles relative to the consensus sequence for all other inferred P. dardanus alleles.

Mentions: Haplotype trees for engrailed exon 1 with synonymous and nonsynonymous changes mapped demonstrate that much of the divergence of the morph-associated alleles from the rest of the P. dardanus alleles is at non-synonymous (replacement) sites (Figure 7). The f. poultoni and f. planemoides alleles are characterised by multiple unique changes, primarily at replacement sites (Figure 7C). Additionally, the f. poultoni and f. planemoides alleles share 3 non-synonymous and 2 synonymous changes. To test for a shared origin of the two divergent alleles, we compared the best tree with an alternative topology in which f. poultoni and f. planemoides were constrained to monophyly. The likelihood of the constrained tree (lnL = -1846.602) was only 0.284 lnL units lower than in the unconstrained tree. This was not a significantly worse (P = 0.98) fit to the data in the SH test, indicating that we cannot rule out a shared origin for these alleles. Unlike the extensive non-synonymous changes in engrailed, all changes within the P. dardanus complex in invected were synonymous.Figure 7


The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus.

Thompson MJ, Timmermans MJ, Jiggins CD, Vogler AP - BMC Evol. Biol. (2014)

The structure of genetic variation in invected and engrailed. Gene trees were established by maximum likelihood for invected (A) and engrailed (B) haplotypes, separately from non-synonymous and synonymous nucleotide changes. Branch lengths correspond to the number of changes. The area of each pie is scaled in proportion to the frequency of that haplotype among the morphs sampled, and colours of pies reflect proportion of haplotypes recovered from each morph, labelled as in Figure 4. (C) Unique SNPs in the two morph-associated alleles relative to the consensus sequence for all other inferred P. dardanus alleles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4262259&req=5

Fig7: The structure of genetic variation in invected and engrailed. Gene trees were established by maximum likelihood for invected (A) and engrailed (B) haplotypes, separately from non-synonymous and synonymous nucleotide changes. Branch lengths correspond to the number of changes. The area of each pie is scaled in proportion to the frequency of that haplotype among the morphs sampled, and colours of pies reflect proportion of haplotypes recovered from each morph, labelled as in Figure 4. (C) Unique SNPs in the two morph-associated alleles relative to the consensus sequence for all other inferred P. dardanus alleles.
Mentions: Haplotype trees for engrailed exon 1 with synonymous and nonsynonymous changes mapped demonstrate that much of the divergence of the morph-associated alleles from the rest of the P. dardanus alleles is at non-synonymous (replacement) sites (Figure 7). The f. poultoni and f. planemoides alleles are characterised by multiple unique changes, primarily at replacement sites (Figure 7C). Additionally, the f. poultoni and f. planemoides alleles share 3 non-synonymous and 2 synonymous changes. To test for a shared origin of the two divergent alleles, we compared the best tree with an alternative topology in which f. poultoni and f. planemoides were constrained to monophyly. The likelihood of the constrained tree (lnL = -1846.602) was only 0.284 lnL units lower than in the unconstrained tree. This was not a significantly worse (P = 0.98) fit to the data in the SH test, indicating that we cannot rule out a shared origin for these alleles. Unlike the extensive non-synonymous changes in engrailed, all changes within the P. dardanus complex in invected were synonymous.Figure 7

Bottom Line: Gene trees for invected do not show this pattern.A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, Natural History Museum, London SW7 5BD, UK. martt@nhm.ac.uk.

ABSTRACT

Background: The phylogenetic history of genes underlying phenotypic diversity can offer insight into the evolutionary origin of adaptive traits. This is especially true where single genes have large phenotypic effects, for example in determining polymorphic mimicry in butterflies. Here, we characterise the evolutionary history of two candidate genes for the mimicry switch in the polymorphic Batesian mimic Papilio dardanus coding for the transcription factors engrailed and invected.

Results: We show that phased haplotypes associated with the dominant morphs f. poultoni and f. planemoides are phylogenetically highly divergent, in particular at non-synonymous sites. Some non-synonymous changes are shared between the divergent alleles suggesting either convergence or a shared ancestry. Gene trees for invected do not show this pattern. Despite their great divergence, all engrailed alleles of P. dardanus were monophyletic with respect to alleles of closely related species. Phylogenetic analyses therefore reveal no evidence for introgression from other species. A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.

Conclusions: The divergence between engrailed haplotypes suggests an evolutionary history distorted by selection with multiple changes reflecting recurrent selective sweeps. The high level of intraspecific polymorphism observed is characteristic of balancing selection on this locus, as expected if the gene engrailed is under phenotypic selection for the maintenance of multiple mimetic morphs. Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.

Show MeSH
Related in: MedlinePlus