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Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps.

ABSTRACT: Numerous studies of emerging species have identified genomic "islands" of elevated differentiation against a background of relative homogeneity. The causes of these islands remain unclear, however, with some signs pointing toward "speciation genes" that locally restrict gene flow and others suggesting selective sweeps that have occurred within nascent species after speciation. Here, we examine this question through the lens of genome sequence data for five species of southern capuchino seedeaters, finch-like birds from South America that have undergone a species radiation during the last ∼50,000 generations. By applying newly developed statistical methods for ancestral recombination graph inference and machine-learning methods for the prediction of selective sweeps, we show that previously identified islands of differentiation in these birds appear to be generally associated with relatively recent, species-specific selective sweeps, most of which are predicted to be soft sweeps acting on standing genetic variation. Many of these sweeps coincide with genes associated with melanin-based variation in plumage, suggesting a prominent role for sexual selection. At the same time, a few loci also exhibit indications of possible selection against gene flow. These observations shed light on the complex manner in which natural selection shapes genome sequences during speciation.

SUBMITTER: Hejase HA

PROVIDER: S-EPMC7720181 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps.

Hejase Hussein A HA Salman-Minkov Ayelet A Campagna Leonardo L Hubisz Melissa J MJ Lovette Irby J IJ Gronau Ilan I Siepel Adam A

Proceedings of the National Academy of Sciences of the United States of America 20201116 48

Numerous studies of emerging species have identified genomic "islands" of elevated differentiation against a background of relative homogeneity. The causes of these islands remain unclear, however, with some signs pointing toward "speciation genes" that locally restrict gene flow and others suggesting selective sweeps that have occurred within nascent species after speciation. Here, we examine this question through the lens of genome sequence data for five species of southern capuchino seedeater ...[more]

PMID: 33199636

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Project description:BackgroundThe páramo ecosystem, located above the timberline in the tropical Andes, has been the setting for some of the most dramatic plant radiations, and it is one of the world's fastest evolving and most diverse high-altitude ecosystems. Today 144+ species of frailejones (subtribe Espeletiinae Cuatrec., Asteraceae) dominate the páramo. Frailejones have intrigued naturalists and botanists, not just for their appealing beauty and impressive morphological diversity, but also for their remarkable adaptations to the extremely harsh environmental conditions of the páramo. Previous attempts to reconstruct the evolutionary history of this group failed to resolve relationships among genera and species, and there is no agreement regarding the classification of the group. Thus, our goal was to reconstruct the phylogeny of the frailejones and to test the influence of the geography on it as a first step to understanding the patterns of radiation of these plants.MethodsField expeditions in 70 páramos of Colombia and Venezuela resulted in 555 collected samples from 110 species. Additional material was obtained from herbarium specimens. Sequence data included nrDNA (ITS and ETS) and cpDNA (rpl16), for an aligned total of 2,954 bp. Fragment analysis was performed with AFLP data using 28 primer combinations and yielding 1,665 fragments. Phylogenies based on sequence data were reconstructed under maximum parsimony, maximum likelihood and Bayesian inference. The AFLP dataset employed minimum evolution analyses. A Monte Carlo permutation test was used to infer the influence of the geography on the phylogeny.ResultsPhylogenies reconstructed suggest that most genera are paraphyletic, but the phylogenetic signal may be misled by hybridization and incomplete lineage sorting. A tree with all the available molecular data shows two large clades: one of primarily Venezuelan species that includes a few neighboring Colombian species; and a second clade of only Colombian species. Results from the Monte Carlo permutation test suggests a very strong influence of the geography on the phylogenetic relationships. Venezuelan páramos tend to hold taxa that are more distantly-related to each other than Colombian páramos, where taxa are more closely-related to each other.ConclusionsOur data suggest the presence of two independent radiations: one in Venezuela and the other in Colombia. In addition, the current generic classification will need to be deeply revised. Analyses show a strong geographic structure in the phylogeny, with large clades grouped in hotspots of diversity at a regional scale, and in páramo localities at a local scale. Differences in the degrees of relatedness between sympatric species of Venezuelan and Colombian páramos may be explained because of the younger age of the latter páramos, and the lesser time for speciation of Espeletiinae in them.

Dataset Information

Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps.

Publications

Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps.

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