Polyphyly and gene flow between non-sibling Heliconius species - PubMed (original) (raw)

Polyphyly and gene flow between non-sibling Heliconius species

Vanessa Bull et al. BMC Biol. 2006.

Abstract

Background: The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America.

Results: In these taxa, we sequenced 30-45 haplotypes per locus of a mitochondrial region containing the genes for cytochrome oxidase subunits I and II (CoI/CoII), and intron-spanning fragments of three unlinked nuclear loci: triose-phosphate isomerase (Tpi), mannose-6-phosphate isomerase (Mpi) and cubitus interruptus (Ci) genes. A fifth gene, dopa decarboxylase (Ddc) produced sequence data likely to be from different duplicate loci in some of the taxa, and so was excluded. Mitochondrial and Tpi genealogies are consistent with reciprocal monophyly, whereas sympatric populations of the species in Panama share identical or similar Mpi and Ci haplotypes, giving rise to genealogical polyphyly at the species level despite evidence for rapid sequence divergence at these genes between geographic races of H. melpomene.

Conclusion: Recent transfer of Mpi haplotypes between species is strongly supported, but there is no evidence for introgression at the other three loci. Our results demonstrate that the boundaries between animal species can remain selectively porous to gene flow long after speciation, and that introgression, even between non-sibling species, can be an important factor in animal evolution. Interspecific gene flow is demonstrated here for the first time in Heliconius and may provide a route for the transfer of switch-gene adaptations for Müllerian mimicry. The results also forcefully demonstrate how reliance on a single locus may give an erroneous picture of the overall genealogical history of speciation and gene flow.

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Figures

Figure 1

Figure 1

Maximum likelihood genealogy for CoI and CoII. Parsimony bootstrap values (>70%) are given above the nodes, taken from the equivalent nodes on the parsimony trees, when available. Major groups of haplotypes, mostly supported by high bootstrap values or indels are identified using Roman numerals. MG = H. melpomene melpomene (French Guiana), MP = H. melpomene rosina (Panama), CP = H. cydno chioneus (Panama), NUM = H. numata.

Figure 2

Figure 2

Maximum likelihood genealogy for Tpi. Parsimony bootstrap values (> 70%) are given above the nodes, taken from the equivalent nodes on the parsimony trees, when available. Insertions or deletions (indels) inferred to be apomorphies are shown using black bars. Indels inferred to be homoplasious or to involve reversals not concordant with the given topologies, are shown as triangles. Major groups of haplotypes, mostly supported by high bootstrap values or indels are identified using Roman numerals. MG = H. melpomene melpomene (French Guiana), MP = H. melpomene rosina (Panama), CP = H. cydno chioneus (Panama), NUM = H. numata.

Figure 3

Figure 3

Maximum likelihood genealogy for Mpi. Parsimony bootstrap values (>70%) are given above the nodes, taken from the equivalent nodes on the parsimony trees, when available. Insertions or deletions (indels) inferred to be apomorphies are shown using black bars. Indels inferred to be homoplasious or to involve reversals not concordant with the given topologies, are shown as triangles. Major groups of haplotypes, mostly supported by high bootstrap values or indels are identified using Roman numeral. MG = H. melpomene melpomene (French Guiana), MP = H. melpomene rosina (Panama), CP = H. cydno chioneus (Panama), NUM = H. numata.

Figure 4

Figure 4

Maximum likelihood genealogy for Ci. Parsimony bootstrap values (>70%) are given above the nodes, taken from the equivalent nodes on the parsimony trees, when available. Insertions or deletions (indels) inferred to be apomorphies are shown using black bars, but indels inferred to be homoplasious or to involve reversals not concordant with the given topologies, are not shown since approximately 27 homoplasious indels would have required showing over 90 gains and losses on the genealogy). This estimated genealogy is poorly resolved and shows many homoplasies, almost certainly due to abundant recombination, and therefore sequence groups were not labeled. MG = H. melpomene melpomene (French Guiana), MP = H. melpomene rosina (Panama), CP = H. cydno chioneus (Panama), NUM = H. numata.

Figure 5

Figure 5

IM analysis of Panama H. melpomene and H. cydno data. The panels show approximate Bayesian posterior probability distributions for effective population size of H. melpomene (θ mel), H. cydno (θ cyd), and the ancestor of the two species (θ A). The time since divergence of the two species (t), and the locus-specific bidirectional introgression rates are also shown (m). The three datasets analysed are the basic IM dataset (blue), and IM reduced dataset 1 (pink) and IM reduced dataset 2 (green). Analysis of the basic IM dataset is compromised by recombination within Tpi and Ci, which is assumed not to occur in the IM algorithm. Reduced datasets containing apparently non-recombined segments of the genes were analyzed to overcome this difficulty. IM reduced dataset 1 differs only from IM reduced dataset 2 in that a different, shorter, part of the Ci locus is used; the low sequence information probably explains why there is little information in the former run in the last panel (probabilities for IM dataset 1 are enhanced 10-fold in this panel only, for clarity). The curves show useful parameter estimation , except in the case of ancestral population size (θ A), the upper tail of the time of divergence (t) and the introgression for Ci for IM reduced dataset 1.

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