An official website of the United States government
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.]
more »
« less
This content will become publicly available on March 25, 2026
Massive Inter-species Introgression Overwhelms Phylogenomic Relationships Among Jaguar, Lion, and Leopard
Abstract Phylogenomic analyses of closely related species allow important glimpses into their evolutionary history. Although recent studies have demonstrated that inter-species hybridization has occurred in several groups, incorporating this process in phylogenetic reconstruction remains challenging. Specifically, the most predominant topology across the genome is often assumed to reflect the speciation tree, but rampant hybridization might overwhelm the genomes, causing that assumption to be violated. The notoriously challenging phylogeny of the 5 extant Panthera species (specifically jaguar [P. onca], lion [P. leo], and leopard [P. pardus]) is an interesting system to address this problem. Here we employed a Panthera-wide whole-genome-sequence data set incorporating 3 jaguar genomes and 2 representatives of lions and leopards to dissect the relationships among these 3 species. Maximum-likelihood trees reconstructed from non-overlapping genomic fragments of 4 different sizes strongly supported the monophyly of all 3 species. The most frequent topology (76–95%) united lion + leopard as a sister species (topology 1), followed by lion + jaguar (topology 2: 4–8%) and leopard + jaguar (topology 3: 0–6%). Topology 1 was dominant across the genome, especially in high-recombination regions. Topologies 2 and 3 were enriched in low-recombination segments, likely reflecting the species tree in the face of hybridization. Divergence times between sister species of each topology, corrected for local-recombination-rate effects, indicated that the lion-leopard divergence was significantly younger than the alternatives, likely driven by post-speciation admixture. Introgression analyses detected pervasive hybridization between lions and leopards, regardless of the assumed species tree. This inference was strongly supported by multispecies-coalescence-with-introgression analyses, which rejected topology 1 (lion+leopard) or any model without introgression. Interestingly, topologies 2 (lion+jaguar) and 3 (jaguar+leopard) with extensive lion-leopard introgression were unidentifiable, highlighting the complexity of this phylogenetic problem. Our results suggest that the dominant genome-wide tree topology is not the true species tree but rather a consequence of overwhelming post-speciation admixture between lion and leopard.
more »
« less
- PAR ID:
- 10618778
- Editor(s):
- Thomson, Robert
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Systematic Biology
- ISSN:
- 1063-5157
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Buerkle, Alex (Ed.)Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species ) . Taxa within Erythranthe , particularly the parapatric and putatively sister species M . lewisii (bee-pollinated) and M . cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M . cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M . lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson’s D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M . lewisii and M . cardinalis . Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M . lewisii and Southern Californian M . parishii each carrying organelle genomes nested within respective sympatric M . cardinalis clades. A recent organellar transfer from M . cardinalis , an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M . parishii organelles in hybrids with M . lewisii . Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.more » « less
-
Abstract Current phylogenomic approaches implicitly assume that the predominant phylogenetic signal within a genome reflects the true evolutionary history of organisms, without assessing the confounding effects of postspeciation gene flow that can produce a mosaic of phylogenetic signals that interact with recombinational variation. Here, we tested the validity of this assumption with a phylogenomic analysis of 27 species of the cat family, assessing local effects of recombination rate on species tree inference and divergence time estimation across their genomes. We found that the prevailing phylogenetic signal within the autosomes is not always representative of the most probable speciation history, due to ancient hybridization throughout felid evolution. Instead, phylogenetic signal was concentrated within regions of low recombination, and notably enriched within large X chromosome recombination cold spots that exhibited recurrent patterns of strong genetic differentiation and selective sweeps across mammalian orders. By contrast, regions of high recombination were enriched for signatures of ancient gene flow, and these sequences inflated crown-lineage divergence times by ∼40%. We conclude that existing phylogenomic approaches to infer the Tree of Life may be highly misleading without considering the genomic architecture of phylogenetic signal relative to recombination rate and its interplay with historical hybridization.more » « less
-
Burbrink, Frank (Ed.)Abstract In cryptic amphibian complexes, there is a growing trend to equate high levels of genetic structure with hidden cryptic species diversity. Typically, phylogenetic structure and distance-based approaches are used to demonstrate the distinctness of clades and justify the recognition of new cryptic species. However, this approach does not account for gene flow, spatial, and environmental processes that can obfuscate phylogenetic inference and bias species delimitation. As a case study, we sequenced genome-wide exons and introns to evince the processes that underlie the diversification of Philippine Puddle Frogs—a group that is widespread, phenotypically conserved, and exhibits high levels of geographically based genetic structure. We showed that widely adopted tree- and distance-based approaches inferred up to 20 species, compared to genomic analyses that inferred an optimal number of five distinct genetic groups. Using a suite of clustering, admixture, and phylogenetic network analyses, we demonstrate extensive admixture among the five groups and elucidate two specific ways in which gene flow can cause overestimations of species diversity: 1) admixed populations can be inferred as distinct lineages characterized by long branches in phylograms; and 2) admixed lineages can appear to be genetically divergent, even from their parental populations when simple measures of genetic distance are used. We demonstrate that the relationship between mitochondrial and genome-wide nuclear $$p$$-distances is decoupled in admixed clades, leading to erroneous estimates of genetic distances and, consequently, species diversity. Additionally, genetic distance was also biased by spatial and environmental processes. Overall, we showed that high levels of genetic diversity in Philippine Puddle Frogs predominantly comprise metapopulation lineages that arose through complex patterns of admixture, isolation-by-distance, and isolation-by-environment as opposed to species divergence. Our findings suggest that speciation may not be the major process underlying the high levels of hidden diversity observed in many taxonomic groups and that widely adopted tree- and distance-based methods overestimate species diversity in the presence of gene flow. [Cryptic species; gene flow; introgression; isolation-by-distance; isolation-by-environment; phylogenetic network; species delimitation.]more » « less
-
ABSTRACT The application of high‐throughput sequencing to phylogenetic analyses is allowing authors to reconstruct the true evolutionary history of species. This work can illuminate specific mechanisms underlying divergence when combined with analyses of gene flow, recombination and selection. We conducted a phylogenomic analysis ofCatharus, a songbird genus with considerable potential for gene flow, variation in migratory behaviour and genomic resources. We documented discordance among trees constructed for mitochondrial, autosomal and sex (Z) chromosome partitions. Two trees were recovered on the Z. Both trees differed from the autosomes, one matched the mitochondria, and the other was unique to the Z. Gene flow with one species likely generated much of this discordance; substantial admixture betweenustulatusand the remaining species was documented and linked to at least two historic events. The tree unique to the Z likely reflects the true history ofCatharus; local genomic analyses recovered the same tree in autosomal regions with reduced admixture and recombination. Genes previously connected to migration were enriched in these regions suggesting transitions between migratory and non‐migratory states helped generate divergence. Migratory (vs. nonmigratory)Catharusformed a monophyletic clade in a subset of genomic regions. Gene flow was elevated in some of these regions suggesting adaptive introgression may have occurred, but the dominant pattern was of balancing selection maintaining ancestral polymorphisms important for olfaction and perhaps, by extension, adaptation to temperate climates. This work illuminates the evolutionary history of an important model in speciation and demonstrates how differential resistance to gene flow can affect local genomic patterns.more » « less
