Extensive Phylogenomic Discordance and the Complex Evolutionary History of the Neotropical Cat Genus Leopardus.

Even in the genomics era, the phylogeny of Neotropical small felids comprised in the genus Leopardus remains contentious. We used whole-genome resequencing data to construct a time-calibrated consensus phylogeny of this group, quantify phylogenomic discordance, test for interspecies introgression, and assess patterns of genetic diversity and demographic history. We infer that the Leopardus radiation started in the Early Pliocene as an initial speciation burst, followed by another in its subgenus Oncifelis during the Early Pleistocene. Our findings challenge the long-held notion that ocelot (Leopardus pardalis) and margay (L. wiedii) are sister species and instead indicate that margay is most closely related to the enigmatic Andean cat (L. jacobita), whose whole-genome data are reported here for the first time. In addition, we found that the newly sampled Andean tiger cat (L. tigrinus pardinoides) population from Colombia associates closely with Central American tiger cats (L. tigrinus oncilla). Genealogical discordance was largely attributable to incomplete lineage sorting, yet was augmented by strong gene flow between ocelot and the ancestral branch of Oncifelis, as well as between Geoffroy's cat (L. geoffroyi) and southern tiger cat (L. guttulus). Contrasting demographic trajectories have led to disparate levels of current genomic diversity, with a nearly tenfold difference in heterozygosity between Andean cat and ocelot, spanning the entire range of variability found in extant felids. Our analyses improved our understanding of the speciation history and diversity patterns in this felid radiation, and highlight the benefits to phylogenomic inference of embracing the many heterogeneous signals scattered across the genome.

Amazonian rivers are leaky barriers to gene flow in forest understory birds.

Ever since Alfred Russel Wallace's nineteenth-century observation that related terrestrial species are often separated on opposing riverbanks, major Amazonian rivers have been recognized as key drivers of speciation. However, rivers are dynamic entities whose widths and courses may vary through time. It thus remains unknown how effective rivers are at reducing gene flow and promoting speciation over long timescales. We fit demographic models to genomic sequences to reconstruct the history of gene flow in three pairs of avian taxa fully separated by different Amazonian rivers, and whose geographic ranges do not make contact in headwater regions where rivers may cease to be barriers. Models with gene flow were best fit but still supported an initial period without any gene flow, which ranged from 187 000 to over 959 000 years, suggesting that rivers are capable of initiating speciation through long stretches of allopatric divergence. Allopatry was followed by either bursts or prolonged episodes of gene flow that retarded genomic differentiation but did not fully homogenize populations. Our results support Amazonian rivers as key barriers that promoted speciation and the build-up of species richness, but they also suggest that river barriers are often leaky, with genomic divergence accumulating slowly owing to episodes of substantial gene flow.

Morphologically cryptic Amazonian bird species pairs exhibit strong postzygotic reproductive isolation.

We possess limited understanding of how speciation unfolds in the most species-rich region of the planet-the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.

Multiple evolutionary units and demographic stability during the last glacial maximum in the Scytalopus speluncae complex (Aves: Rhinocryptidae).

The Atlantic Forest (AF) of South America harbors one of the world's highest bird species richness, but to date there is a deficient understanding of the spatial patterns of genetic diversity and the evolutionary history of this biome. Here we estimated the phylogenetic and populational history of the widespread Mouse-colored Tapaculo (Scytalopus speluncae) complex across the Brazilian AF, using data from two mitochondrial genes and 12 microsatellite loci. Both markers uncovered several cryptic, mostly allopatric and well-supported lineages that may represent distinct species-level taxa. We investigated whether diversification in S. speluncae is compatible with the Carnaval-Moritz model of Pleistocene refugia. We found that northern lineages have high levels of genetic diversity, agreeing with predictions of more stable forest refugia in these areas. In contrast, southern lineages have lower levels of mtDNA diversity with a signature of population expansion that occurred earlier (∼0.2Mya) than the last glacial maximum. This result suggests that the AF may be stable enough to maintain endemic taxa through glacial cycles. Moreover, we propose that the "mid-Pleistocene climate transition" between 1.2 and 0.7million years ago, from a warmer to a colder climate, may have played an important but mostly overlooked role in the evolution of AF montane taxa.

Genomic data reveal a protracted window of introgression during the diversification of a neotropical woodcreeper radiation.

The incidence of introgression during the diversification process and the timespan following divergence when introgression is possible are poorly understood in the neotropics where high species richness could provide extensive opportunities for genetic exchange. We used thousands of genome-wide SNPs to infer phylogenetic relationships, calculate ages of splitting, and to estimate the timing of introgression in a widespread avian neotropical genus of woodcreepers. Five distinct introgression events were reconstructed involving taxa classified both as subspecies and species including lineages descending from the basal-most split, dated to 7.3 million years ago. Introgression occurred between just a few hundred thousand to about 2.5 million years following divergence, suggesting substantial portions of the genome are capable of introgressing across taxa boundaries during a protracted time window of a few million years following divergence. Despite this protracted time window, we found that the proportion of the genome introgressing (6-11%) declines with the time of introgression following divergence, suggesting that the genome becomes progressively more immune to introgression as reproductive isolation increases.

A new species of Caecilia (Gymnophiona, Caeciliidae) from the Magdalena valley region of Colombia.

A new species of the genus Caecilia (Caeciliidae) from the western foothills of the Serranía de los Yariguíes in Colombia is described. Caecilia pulchraserrana sp. nov. is similar to C. degenerata and C. corpulenta but differs from these species in having fewer primary annular grooves and a shorter body length. With this new species, the currently recognized species in the genus are increased to 35. Mitochondrial DNA sequences, including newly sequenced terminals representing two additional, previously unanalyzed species, corroborate the phylogenetic position of the new species within Caecilia and the monophyly of the genus. This analysis also included newly sequenced terminals of Epicrionops aff. parkeri (Rhinatrematidae) and trans-Andean Microcaecilia nicefori (Siphonopidae). Evidence was found for the non-monophyly of the family Siphonopidae and the siphonopid genera Microcaecilia and Siphonops. The implications of these results for caecilian systematics are discussed and the status of the trans-Andean populations of Caecilia degenerata is commented upon.

Extinction as a driver of avian latitudinal diversity gradients.

The role of historical factors in driving latitudinal diversity gradients is poorly understood. Here, we used an updated global phylogeny of terrestrial birds to test the role of three key historical factors-speciation, extinction, and dispersal rates-in generating latitudinal diversity gradients for eight major clades. We fit a model that allows speciation, extinction, and dispersal rates to differ, both with latitude and between the New and Old World. Our results consistently support extinction (all clades had lowest extinction where species richness was highest) as a key driver of species richness gradients across each of eight major clades. In contrast, speciation and dispersal rates showed no consistent latitudinal patterns across replicate bird clades, and thus are unlikely to represent general underlying drivers of latitudinal diversity gradients.

Hybridization in headwater regions, and the role of rivers as drivers of speciation in Amazonian birds.

Many understory birds and other groups form genetically differentiated subspecies or closely related species on opposite sides of major rivers of Amazonia, but are proposed to come into geographic contact in headwater regions where narrower river widths may present less of a dispersal barrier. Whether such forms hybridize in headwater regions is generally unknown, but has important implications to our understanding of the role of rivers as drivers of speciation. We used a dataset of several thousand single nucleotide polymorphisms to show that seven taxon pairs that differentiate across a major Amazonian river come into geographic contact and hybridize in headwater regions. All taxon pairs possessed hybrids with low numbers of loci in which alleles were inherited from both parental species, suggesting they are backcrossed with parentals, and indicating gene flow between parental populations. Ongoing gene flow challenges rivers as the sole cause of in situ speciation, but is compatible with the view that the wide river courses in the heart of Amazonia may have driven interfluvial divergence during episodes of wet forest retraction away from headwater regions. Taxa as old as 4 Ma in our Amazonian dataset continue to hybridize at contact zones, suggesting reproductive isolation evolves at a slow pace.