Controversies in evolutionary biology can linger for centuries. This is not because evolutionary biologists are unusually contentious, but rather because evolution is a challenging science that involves the reconstruction of events tracing back more than 3.7 billion years. Also, evolutionary processes common to one organismal group may be absent in another. Thus, generalizations about evolution must be built on studies of many taxa, with the recognition that exceptions to every rule are likely. Given these challenges, celebrations should be had when major controversies are put to rest. On page 594 of this issue, Edelman et al. (1) help bring one such controversy to a close by demonstrating the importance of hybridization (interbreeding between species) in the diversification of Heliconius butterflies. They also develop a new technique to disentangle genomic patterns caused by hybridization from those caused by stochastic processes within species.

The controversy about the role of hybridization in evolution began almost 300 years ago when the Swedish botanist Carl Linnaeus posited that new forms of plants could arise by hybridization (2). This suggestion was criticized by members of the clergy because it challenged the immutability of species. Darwin (3) also expressed skepticism about the importance of hybridization, albeit for scientific reasons. In the 20th century, the prevailing view among evolutionary biologists aligned closely with Darwin’s, holding that hybridization was rare, and when it did occur, it was likely to be maladaptive and transitory, leading either to the completion of speciation or to the merging of hybridizing entities (45). The alternative view held that hybridization was more common than generally appreciated, but even when rare, it could provide useful genetic variation that could be exploited through natural selection (6).


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Variation in wing patterns in Heliconius butterflies defines different species, which often have admixed genomes.




With fully sequenced genomes now available for many organisms, as well as methods for detecting the genomic signatures of past hybridization events (7), it is now possible to assess both the presence and genomic extent of admixture (the presence of DNA in an individual that derives from distantly related lineages, often due to hybridization). Admixture has been detected in numerous genomes across the domains of life, including more than 70 cases where it is known to be adaptive (enhance evolutionary fitness) (8). The extent of genetic exchange is such that some biologists have argued that the use of trees for depictions of the history of life should be abandoned in favor of networks, which can depict both branching and reticulate evolutionary histories (9).

Heliconius butterflies are endemic to tropical America and comprise ∼40 species, which are known for the spectacular diversity (and beauty) of their wing patterns (see the photo). The colorful wing patterns not only warn predators of a butterfly’s distastefulness, they also offer cues for mate recognition, which contributes to speciation by promoting breeding within species. Hybridization underlies the origin and exchange of wing patterns, aiding the establishment of new hybrid species (10), as well as the evolution of Müllerian mimics (11), in which different unpalatable species share similar warning wing patterns. However, these inferences have been questioned (12), partly because of technical difficulties in distinguishing between admixture (hybridization) and the stochastic sorting of ancestral polymorphisms, called incomplete lineage sorting (ILS). The latter occurs when there is not enough time for genetic drift to resolve polymorphic loci (that is, the extinction of all but one allele at a locus) prior to the next speciation event. Consequently, genealogies frequently differ from the species phylogeny, imitating phylogenomic patterns caused by hybridization.

To estimate the importance of hybridization and introgression (interspecific genetic exchange by hybridization) in Heliconius, Edelman et al. generated 20 new genome assemblies for Heliconius species and related genera. The authors then determined the genealogies of loci from across the Heliconius genome. Most genealogies were incongruent: They differed from each other and from a consensus “species” phylogeny for the group, suggesting that ILS and/or admixture were common.

To distinguish between these possibilities, Edelman et al. developed a new method called “quantifying introgression via branch lengths” (QuIBL). The method takes advantage of the observation that the internal branch lengths in a genealogy are expected to be longer on average if incongruence is due to introgression rather than ILS. Extensive simulations over a wide range of demographic conditions indicate that this method is more accurate than previous approaches. When applied to small genomic regions across 13 Heliconius genomes, ∼20% of genomic windows were estimated to have a history of introgression, and ů70% of incongruent genealogies were due to introgression compared with 30% from ILS. This implies that even when speciation events occur close together in time, such as in rapidly diversifying groups, hybridization rather than ILS is the dominant cause of genealogical incongruence.

So, is the observed extensive introgression of evolutionary importance? Analyses of the genomic distribution of introgressions indicate that they are associated with high recombination rates. This distribution implies that most introgressions probably are maladaptive (13). Recombination can remove harmful alleles from introgressions (leaving neutral fragments behind) before they are eliminated from the genome by natural selection. The authors also report a new chromosomal inversion that likely represents an example of adaptive introgression. Inversions typically suppress recombination in heterozygotes and can aid adaptive divergence and speciation by preventing combinations of adaptive alleles from being broken up by recombination. This particular inversion includes the cortex locus, which underlies the evolution of wing coloration patterns and mimicry in another Heliconius species (14). Thus, introgression likely has had both harmful and beneficial consequences in Heliconius.

The study of Edelman et al. adds to a growing literature indicating that the footprints of hybridization are a common feature of plant and animal genomes and that hybridization can provide the fuel for adaptive diversification. However, this does not necessarily mean that hybridization is common at the population level. For example, a single successful hybridization event early in the divergence of a lineage could leave traces in all descendants. Thus, an important next step is to estimate the number and diversity of hybridization events required to account for observed patterns of genomic admixture.



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