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Abstract Can knowledge about genome architecture inform biogeographic and phylogenetic inference? Selection, drift, recombination, and gene flow interact to produce a genomic landscape of divergence wherein patterns of differentiation and genealogy vary nonrandomly across the genomes of diverging populations. For instance, genealogical patterns that arise due to gene flow should be more likely to occur on smaller chromosomes, which experience high recombination, whereas those tracking histories of geographic isolation (reduced gene flow caused by a barrier) and divergence should be more likely to occur on larger and sex chromosomes. In Amazonia, populations of many bird species diverge and introgress across rivers, resulting in reticulated genomic signals. Herein, we used reduced representation genomic data to disentangle the evolutionary history of 4 populations of an Amazonian antbird, Thamnophilus aethiops, whose biogeographic history was associated with the dynamic evolution of the Madeira River Basin. Specifically, we evaluate whether a large river capture event ca. 200 Ka, gave rise to reticulated genealogies in the genome by making spatially explicit predictions about isolation and gene flow based on knowledge about genomic processes. We first estimated chromosome-level phylogenies and recovered 2 primary topologies across the genome. The first topology (T1) was most consistent with predictions about population divergence and was recovered for the Z-chromosome. The second (T2), was consistent with predictions about gene flow upon secondary contact. To evaluate support for these topologies, we trained a convolutional neural network to classify our data into alternative diversification models and estimate demographic parameters. The best-fit model was concordant with T1 and included gene flow between non-sister taxa. Finally, we modeled levels of divergence and introgression as functions of chromosome length and found that smaller chromosomes experienced higher gene flow. Given that (1) genetrees supporting T2 were more likely to occur on smaller chromosomes and (2) we found lower levels of introgression on larger chromosomes (and especially the Z-chromosome), we argue that T1 represents the history of population divergence across rivers and T2 the history of secondary contact due to barrier loss. Our results suggest that a significant portion of genomic heterogeneity arises due to extrinsic biogeographic processes such as river capture interacting with intrinsic processes associated with genome architecture. Future phylogeographic studies would benefit from accounting for genomic processes, as different parts of the genome reveal contrasting, albeit complementary histories, all of which are relevant for disentangling the intricate geogenomic mechanisms of biotic diversification. [Amazonia; biogeography; demographic modeling; gene flow; gene tree; genome architecture; geogenomics; introgression; linked selection; neural network; phylogenomic; phylogeography; reproductive isolation; speciation; species tree.]
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Varied diversification patterns and distinct demographic trajectories in Ethiopian montane forest bird (Aves: Passeriformes) populations separated by the Great Rift Valley
Abstract Taxon‐specific characteristics and extrinsic climatic and geological forces may both shape population differentiation and speciation. In geographically and taxonomically focused investigations, differentiation may occur synchronously as species respond to the same external conditions. Conversely, when evolution is investigated in taxa with largely varying traits, population differentiation and speciation is complex and shaped by interactions of Earth's template and species‐specific traits. As such, it is important to characterize evolutionary histories broadly across the tree of life, especially in geographic regions that are exceptionally diverse and under pressures from human activities such as in biodiversity hotspots. Here, using whole‐genome sequencing data, we characterize genomic variation in populations of six Ethiopian Highlands forest bird species separated by a lowland biogeographic barrier, the Great Rift Valley (GRV). In all six species, populations on either side of the GRV exhibited significant but varying levels of genetic differentiation. Species’ dispersal ability was negatively correlated with levels of population differentiation. Isolation with migration models indicated varied patterns of population differentiation and connectivity among populations of the focal species. We found that demographic histories—estimated for each individual—varied by both species and population but were consistent between individuals of the same species and sampling region. We found that genomic diversity varied by half an order of magnitude across species, and that this variation could largely be explained by the harmonic mean of effective population size over the past 200,000 years. Overall, we found that even in highly dispersive species like birds, the GRV acts as a substantial biogeographic barrier.
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- Award ID(s):
- 1953688
- PAR ID:
- 10366516
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 31
- Issue:
- 9
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 2664-2678
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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