Genomic evidence of speciation reversal in ravens

Abstract

Many species, including humans, have emerged via complex reticulate processes involving hybridisation. Under certain circumstances, hybridisation can cause distinct lineages to collapse into a single lineage with an admixed mosaic genome. Most known cases of such ‘speciation reversal’ or ‘lineage fusion’ involve recently diverged lineages and anthropogenic perturbation. Here, we show that in western North America, Common Ravens (Corvus corax) have admixed mosaic genomes formed by the fusion of non-sister lineages (‘California’ and ‘Holarctic’) that diverged ~1.5 million years ago. Phylogenomic analyses and concordant patterns of geographic structuring in mtDNA, genome-wide SNPs and nuclear introns demonstrate long-term admixture and random interbreeding between the non-sister lineages. In contrast, our genomic data support reproductive isolation between Common Ravens and Chihuahuan Ravens (C. cryptoleucus) despite extensive geographic overlap and a sister relationship between Chihuahuan Ravens and the California lineage. These data suggest that the Common Raven genome was formed by secondary lineage fusion and most likely represents a case of ancient speciation reversal that occurred without anthropogenic causes.

A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris

“…Despeciation and lineage fusion driven by the isolation and secondary contact mechanism leading to mitonuclear discordance may also have happened in other organisms, especially in those that at present display high population numbers and important levels of gene flow. For example, a recent case has been described in birds (Kearns et al, ). In widescale DNA barcoding surveys, highly diverged mtDNA haplotypes are sometimes detected at low frequency and scattered across the range of common species, as in the butterfly Melitaea didyma (Esper, 1778) (Pazhenkova & Lukhtanov, ).…”

Cryptic and extensive hybridization between ancient lineages of American crows

“…During the interglacial periods, terrestrial organisms expanded from refugial populations into newly ice‐free habitats, leading to secondary contact and potentially renewed gene flow between closely related, previously allopatric forms (Shafer et al, 2010). These repeated cycles of isolation and secondary contact created complex and/or reticulate population genetic histories in many of the region's terrestrial organisms (Hewitt, 2004; Kearns et al, 2018; Latch, Heffelfinger, Fike, & Rhodes, 2009; Omland, Tarr, Boarman, Marzluff, & Fleischer, 2000).…”

“…By comparison, much less is known about what is happening in cryptic hybrid zones, and research on this topic has begun to appear only recently (e.g., Herrera‐Aguilar et al, 2009; Patel, Schell, Eifert, Feldmeyer, & Pfenninger, 2015; Pfenninger & Nowak, 2008; Pulido‐Santacruz et al, 2018; Quilodrán, Austerlitz, Currat, & Montoya‐Burgos, 2018). These few studies have already documented a variety of evolutionary patterns and processes operating in the absence of morphological differences, including cryptic reticulate evolution (Kearns et al, 2018). However, additional genomic studies of cryptic hybrid zones are needed to better synthesize how evolutionary processes may differ at hybrid zones with and without substantial morphological differentiation.…”

Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis)

“…Given this history of the field, unusual mtDNA patterns have often been submitted as compelling evidence for rare historical events (e.g., historical isolation followed by admixture); however, our simulations show that in species with large effective population sizes, conventional interpretations of mtDNA patterns may be particularly misleading. In these cases, it will be impossible to tease apart different demographic hypotheses in the absence of corroborating data (e.g., Kearns et al, ). Second, recent population separation and high migration rate are common explanations for the absence of population differentiation in species; however, our results along with other bird species (e.g., Hung et al, ) and many marine fish species (e.g., Cano, Shikano, Kuparinen, & Merilä, ) indicate that effective population size may also be an important population genetic parameter influencing patterns of population differentiation at neutral loci.…”

“…Given this history of the field, unusual mtDNA patterns have often been submitted as compelling evidence for rare historical events (e.g., historical isolation followed by admixture); however, our simulations show that in species with large effective population sizes, conventional interpretations of mtDNA patterns may be particularly misleading. In these cases, it will be impossible to tease apart different demographic hypotheses in the absence of corroborating data (e.g., Kearns et al, 2018).…”