Gene flow persists millions of years after speciation in Heliconius butterflies - PubMed (original) (raw)

Gene flow persists millions of years after speciation in Heliconius butterflies

Marcus R Kronforst. BMC Evol Biol. 2008.

Abstract

Background: Hybridization, or the interbreeding of two species, is now recognized as an important process in the evolution of many organisms. However, the extent to which hybridization results in the transfer of genetic material across the species boundary (introgression) remains unknown in many systems, as does the length of time after initial divergence that the species boundary remains porous to such gene flow.

Results: Here I use genome-wide genotypic and DNA sequence data to show that there is introgression and admixture between the melpomene/cydno and silvaniform clades of the butterfly genus Heliconius, groups that separated from one another as many as 30 million generations ago. Estimates of historical migration based on 523 DNA sequences from 14 genes suggest unidirectional gene flow from the melpomene/cydno clade into the silvaniform clade. Furthermore, genetic clustering based on 520 amplified fragment length polymorphisms (AFLPs) identified multiple individuals of mixed ancestry showing that introgression is on-going.

Conclusion: These results demonstrate that genomes can remain porous to gene flow very long after initial divergence. This, in turn, greatly expands the evolutionary potential afforded by introgression. Phenotypic and species diversity in a wide variety of organisms, including Heliconius, have likely arisen from introgressive hybridization. Evidence for continuous gene flow over millions of years points to introgression as a potentially important source of genetic variation to fuel the evolution of novel forms.

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Figures

Figure 1

Figure 1

Bayesian phylogeny showing the relationship between the distantly-related silvaniform and melpomene/cydno clades of the genus Heliconius. Posterior probabilities for three major nodes are shown (1.0), as are the wing pattern phenotypes for the four analyzed species. The age of the split between the melpomene/cydno and silvaniform clades was estimated assuming an evolutionary rate of 1.15% per lineage per million years [32].

Figure 2

Figure 2

Posterior probability distributions for between-species population migration rates. Three pairwise comparisons based on DNA sequence data for 14 genes revealed non-zero rates of historical gene flow from the melpomene/cydno clade into the silvaniform clade (a, b, c). Locus specific estimates of gene flow into H. hecale from H. melpomene, H. pachinus, and H. cydno, respectively, for the two loci that exhibit evidence of between-clade introgression, cubitus interruptus and white (d, e, f).

Figure 3

Figure 3

Marginal posterior probability distributions for locus-specific migration rates. Probability distributions for gene flow from H. hecale into H. melpomene, H. pachinus, and H. cydno, respectively (a, b, c). Probability distributions for gene flow into H. hecale from H. melpomene, H. pachinus, and H. cydno, respectively (d, e, f). Despite substantial variation in distribution shapes, most peak at or near zero suggestive of little or no gene flow.

Figure 4

Figure 4

Gene genealogies for cubitus interruptus and white. Across loci, haplotypes from H. hecale and the melpomene/cydno clade were reciprocally monophyletic except for at cubitus interruptus and white [24]. The lack of association between species and tree topology for these two loci is indicative of interspecific gene flow. Nodes with posterior probabilities > 0.60 are labeled.

Figure 5

Figure 5

Genetic clustering based on 520 AFLP loci. Each individual is represented by a narrow vertical column with the proportion of the four colors indicating the genome proportion derived from each of the four populations. Two H. hecale and two H. cydno individuals exhibited evidence of mixed ancestry with the opposite clade (asterisks).

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