Range-wide phylogenomics of the Great Horned Owl (Bubo virginianus) reveals deep north-south divergence in northern Peru.

The Great Horned Owl (Bubo virginianus) inhabits myriad habitats throughout the Americas and shows complex patterns of individual and geographic morphological variation. The owl family Strigidae is known to follow ecogeographic rules, such as Gloger's rule. Although untested at the species level, these ecogeographic rules may affect B. virginianus plumage coloration and body size. Previous studies have indicated that, despite this species' morphological variability, little genetic differentiation exists across parts of their range. This study uses reduced representation genome-wide nuclear and complete mitochondrial DNA sequence data to assess range-wide relationships among B. virginianus populations and the disputed species status of B. v. magellanicus (Magellanic or Lesser Horned Owl) of the central and southern Andes. We found shallow phylogenetic relationships generally structured latitudinally to the north of the central Andes, and a deep divergence between a southern and northern clade close to the Marañón Valley in the central Andes, a common biogeographic barrier. We identify evidence of gene flow between B. v. magellanicus and other subspecies based on mitonuclear discordance and F-branch statistics. Overall differences in morphology, plumage coloration, voice, and genomic divergence support species status for B. v. magellanicus.

Finding complexity in complexes: Assessing the causes of mitonuclear discordance in a problematic species complex of Mesoamerican toads.

Mitonuclear discordance is a frequently encountered pattern in phylogeographic studies and occurs when mitochondrial and nuclear DNA display conflicting signals. Discordance among these genetic markers can be caused by several factors including confounded taxonomies, gene flow, and incomplete lineage sorting. In this study, we present a strong case of mitonuclear discordance in a species complex of toads (Bufonidae: Incilius coccifer complex) found in the Chortís Block of Central America. To determine the cause of mitonuclear discordance in this complex, we used spatially explicit genetic data to test species limits and relationships, characterize demographic history, and quantify gene flow. We found extensive mitonuclear discordance among the three recognized species within this group, especially in populations within the Chortís Highlands of Honduras. Our data reveal nuclear introgression within the Chortís Highlands populations that was most probably driven by cyclical range expansions due to climatic fluctuations. Though we determined introgression occurred within the nuclear genome, our data suggest that it is not the key factor in driving mitonuclear discordance in the entire species complex. Rather, due to a lack of discernible geographic pattern between mitochondrial and nuclear DNA, as well as a relatively recent divergence time of this complex, we concluded that mitonuclear discordance has been caused by incomplete lineage sorting. Our study provides a framework to test sources of mitonuclear discordance and highlights the importance of using multiple marker types to test species boundaries in cryptic species.

Comparative phylogeography of trans-Andean freshwater fishes based on genome-wide nuclear and mitochondrial markers.

The Neotropical region represents one of the greatest biodiversity hot spots on earth. Despite its unparalleled biodiversity, regional comparative phylogeographic studies are still scarce, with most focusing on model clades (e.g. birds) and typically examining a handful of loci. Here, we apply a genome-wide comparative phylogeographic approach to test hypotheses of codiversification of freshwater fishes in the trans-Andean region. Using target capture methods, we examined exon data for over 1,000 loci combined with complete mitochondrial genomes to study the phylogeographic history of five primary fish species (>150 individuals) collected from eight major river basins in Northwestern South America and Lower Central America. To assess their patterns of genetic structure, we inferred genealogical concordance taking into account all major aspects of phylogeography (within loci, across multiple genes, across species and among biogeographic provinces). Based on phylogeographic concordance factors, we tested four a priori biogeographic hypotheses, finding support for three of them and uncovering a novel, unexpected pattern of codiversification. The four emerging inter-riverine patterns are as follows: (a) Tuira + Atrato, (b) Ranchería + Catatumbo, (c) Magdalena system and (d) Sinú + Atrato. These patterns are interpreted as shared responses to the complex uplifting and orogenic processes that modified or sundered watersheds, allowing codiversification and speciation over geological time. We also find evidence of cryptic speciation in one of the species examined and instances of mitochondrial introgression in others. These results help further our knowledge of the historical geographic factors shaping the outstanding biodiversity of the Neotropics.

Strong Amerindian Mitonuclear Discordance in Puerto Rican Genomes Suggests Amerindian Mitochondrial Benefit.

A large discrepancy between the Amerindian contribution to the mitochondrial and nuclear genetic components of 55 Puerto Rican (PR) genomes from the 1000 Genomes Project is identified, with Amerindian mitochondrial haplotypes being highly represented (67.3%), in strong contrast to the Amerindian autosomal contribution (12.9%). I examine the potential causes behind this strong mitonuclear discordance. The Amerindian contribution to the X chromosome is 19.8%, implying assortative mating with Amerindian females during the establishment of the PR population. However, this scenario does not account for the extraordinarily high Amerindian mitochondrial contribution. Demographic simulation of simple assortative mating scenarios during establishment of the PR population indicates that the observed Amerindian mitochondrial contribution is higher than expected. The simulations show that expansion from a small founding population does not produce the observed frequencies, instead producing the frequencies expected under neutrality, with the Amerindian mitochondrial frequencies approximately twice the Amerindian autosomal proportion. In addition, multiple replicated simulations show that drift is an unlikely explanation for the elevated Amerindian mitochondrial frequency, as these are unable to produce the elevated Amerindian mitochondrial frequency observed in the PR genomic dataset, under a range of different starting conditions. I conclude that the mitonuclear discordance appears most consistent with adaptive mitochondrial benefit; however, the molecular mechanism(s) remain to be characterized before this can be confirmed and warrant further investigation. Lastly, I show potential evidence of selection on autosomes and allosomes, using admixture proportions. Interestingly, the major histocompatibility complex locus on chromosome 6 shows greatly elevated single nucleotide polymorphism density but is unaccompanied by strong admixture variance. The observations on mitonuclear discordance may affect the interpretation of apparent assortative mating in recent human admixture events, which should be treated with caution when relying only on mitochondrial haplotype frequencies.

Genetic surfing, not allopatric divergence, explains spatial sorting of mitochondrial haplotypes in venomous coralsnakes.

Strong spatial sorting of genetic variation in contiguous populations is often explained by local adaptation or secondary contact following allopatric divergence. A third explanation, spatial sorting by stochastic effects of range expansion, has been considered less often though theoretical models suggest it should be widespread, if ephemeral. In a study designed to delimit species within a clade of venomous coralsnakes, we identified an unusual pattern within the Texas coral snake (Micrurus tener): strong spatial sorting of divergent mitochondrial (mtDNA) lineages over a portion of its range, but weak sorting of these lineages elsewhere. We tested three alternative hypotheses to explain this pattern-local adaptation, secondary contact following allopatric divergence, and range expansion. Collectively, near panmixia of nuclear DNA, the signal of range expansion associated sampling drift, expansion origins in the Gulf Coast of Mexico, and species distribution modeling suggest that the spatial sorting of divergent mtDNA lineages within M. tener has resulted from genetic surfing of standing mtDNA variation-not local adaptation or allopatric divergence. Our findings highlight the potential for the stochastic effects of recent range expansion to mislead estimations of population divergence made from mtDNA, which may be exacerbated in systems with low vagility, ancestral mtDNA polymorphism, and male-biased dispersal.