Recombination-Aware Phylogenomics Reveals the Structured Genomic Landscape of Hybridizing Cat Species

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.

Genomic patterns in the widespread Eurasian lynx shaped by Late Quaternary climatic fluctuations and anthropogenic impacts

“…For PCA, and also pairwise genetic distances and admixture analyses we set a SNP_pval of 1e−3. The resulting PCA was plotted using scatterplot3js from threejs library in R (Lewis, 2017). PCA coordinates were scaled to geographical coordinates (Procrustes analysis, following Borg & Groenen, 1997) to assess similarities between geographical and genetic distribution using the package mcmcpack (Martin, Quinn, & Park, 2011) in R (R Core Team 2019).…”

“…The species suffered a massive demographic decline registered by PSMC between 3 Mya and 200 kya (Figure 2a), which may reflect a founder effect associated with the speciation from a common ancestor of Eurasian and Canada lynxes (recently dated around 1-1.2 Mya; Li, Figueiró, Eizirik, & Murphy, 2019). Low species-wide genetic diversity, which is comparable to that of the white African lion or Greenlandic brown bear ( Figure S16), might be-at least partiallythe long-term consequence of this drastic reduction in population size (Frankham, 2015;Frankham et al, 2011).…”

Admixture in Mammals and How to Understand Its Functional Implications

“…Molecular data have also revealed hybrid zones between related wild species, for example, lynx and bobcat (Table S2, Supporting Information). Nuclear genomic data suggest that gene flow may be common among species in the ocelot, Asian leopard, and Panthera lineages, and recently, whole‐genome sequences of Panthera have revealed multiple instances of introgression …”

Ghost Introgression: Spooky Gene Flow in the Distant Past

“…Similarly, ghost introgression might explain rapid diversification events in other mammalian groups, such as horses, [ 40 ] elephants, [ 41 ] and cats. [ 42 ]…”