Peter A. Hosner

Tectonic collision and uplift of Wallacea triggered the global songbird radiation

Songbirds (oscine passerines) are the most species-rich and cosmopolitan bird group, comprising almost half of global avian diversity. Songbirds originated in Australia, but the evolutionary trajectory from a single species in an isolated continent to worldwide proliferation is poorly understood. Here, we combine the first comprehensive genome-scale DNA sequence data set for songbirds, fossil-based time calibrations, and geologically informed biogeographic reconstructions to provide a well-supported evolutionary hypothesis for the group. We show that songbird diversification began in the Oligocene, but accelerated in the early Miocene, at approximately half the age of most previous estimates. This burst of diversification occurred coincident with extensive island formation in Wallacea, which provided the first dispersal corridor out of Australia, and resulted in independent waves of songbird expansion through Asia to the rest of the globe. Our results reconcile songbird evolution with Earth history and link a major radiation of terrestrial biodiversity to early diversification within an isolated Australian continent.

Avoiding missing data biases in phylogenomic inference: an empirical study in the landfowl (Aves: Galliformes)

Production of massive DNA sequence data sets is transforming phylogenetic inference, but best practices for analyzing such data sets are not well established. One uncertainty is robustness to missing data, particularly in coalescent frameworks. To understand the effects of increasing matrix size and loci at the cost of increasing missing data, we produced a 90 taxon, 2.2 megabase, 4,800 locus sequence matrix of landfowl using target capture of ultraconserved elements. We then compared phylogenies estimated with concatenated maximum likelihood, quartet-based methods executed on concatenated matrices and gene tree reconciliation methods, across five thresholds of missing data. Results of maximum likelihood and quartet analyses were similar, well resolved, and demonstrated increasing support with increasing matrix size and sparseness. Conversely, gene tree reconciliation produced unexpected relationships when we included all informative loci, with certain taxa placed toward the root compared with other approaches. Inspection of these taxa identified a prevalence of short average contigs, which potentially biased gene tree inference and caused erroneous results in gene tree reconciliation. This suggests that the more problematic missing data in gene tree-based analyses are partial sequences rather than entire missing sequences from locus alignments. Limiting gene tree reconciliation to the most informative loci solved this problem, producing well-supported topologies congruent with concatenation and quartet methods. Collectively, our analyses provide a well-resolved phylogeny of landfowl, including strong support for previously problematic relationships such as those among junglefowl (Gallus), and clarify the position of two enigmatic galliform genera (Lerwa, Melanoperdix) not sampled in previous molecular phylogenetic studies.

Why Do Phylogenomic Data Sets Yield Conflicting Trees? Data Type Influences the Avian Tree of Life more than Taxon Sampling

&NA; Phylogenomics, the use of large‐scale data matrices in phylogenetic analyses, has been viewed as the ultimate solution to the problem of resolving difficult nodes in the tree of life. However, it has become clear that analyses of these large genomic data sets can also result in conflicting estimates of phylogeny. Here, we use the early divergences in Neoaves, the largest clade of extant birds, as a “model system” to understand the basis for incongruence among phylogenomic trees. We were motivated by the observation that trees from two recent avian phylogenomic studies exhibit conflicts. Those studies used different strategies: 1) collecting many characters [∼ 42 mega base pairs (Mbp) of sequence data] from 48 birds, sometimes including only one taxon for each major clade; and 2) collecting fewer characters (∼ 0.4 Mbp) from 198 birds, selected to subdivide long branches. However, the studies also used different data types: the taxon‐poor data matrix comprised 68% non‐coding sequences whereas coding exons dominated the taxon‐rich data matrix. This difference raises the question of whether the primary reason for incongruence is the number of sites, the number of taxa, or the data type. To test among these alternative hypotheses we assembled a novel, large‐scale data matrix comprising 90% non‐coding sequences from 235 bird species. Although increased taxon sampling appeared to have a positive impact on phylogenetic analyses the most important variable was data type. Indeed, by analyzing different subsets of the taxa in our data matrix we found that increased taxon sampling actually resulted in increased congruence with the tree from the previous taxon‐poor study (which had a majority of non‐coding data) instead of the taxon‐rich study (which largely used coding data). We suggest that the observed differences in the estimates of topology for these studies reflect data‐type effects due to violations of the models used in phylogenetic analyses, some of which may be difficult to detect. If incongruence among trees estimated using phylogenomic methods largely reflects problems with model fit developing more “biologically‐realistic” models is likely to be critical for efforts to reconstruct the tree of life. [Birds; coding exons; GTR model; model fit; Neoaves; non‐coding DNA; phylogenomics; taxon sampling.]

CLIMATE-DRIVEN DIVERSIFICATION AND PLEISTOCENE REFUGIA IN PHILIPPINE BIRDS: EVIDENCE FROM PHYLOGEOGRAPHIC STRUCTURE AND PALEOENVIRONMENTAL NICHE MODELING

Avian diversification in oceanic archipelagos is largely attributed to isolation across marine barriers. During glacial maxima, lowered sea levels resulted in repeated land connections between islands joined by shallow seas. Consequently, such islands are not expected to show endemism. However, if climate fluctuations simultaneously caused shifts in suitable environmental conditions, limiting populations to refugia, then occurrence on and dispersal across periodic land bridges are not tenable. To assess the degree to which paleoclimate barriers, rather than marine barriers, drove avian diversification in the Philippine Archipelago, we produced ecological niche models for current‐day, glacial maxima, and interglacial climate scenarios to infer potential Pleistocene distributions and paleoclimate barriers. We then tested marine and paleoclimate barriers for correspondence to geographic patterns of population divergence, inferred from DNA sequences from eight codistributed bird species. In all species, deep‐water channels corresponded to zones of genetic differentiation, but six species exhibited deeper divergence associated with a periodic land bridge in the southern Philippines. Ecological niche models for these species identified a common paleoclimate barrier that coincided with deep genetic structure among populations. Although dry land connections joined southern Philippine islands during low sea level stands, unfavorable environmental conditions limited populations within landmasses, resulting in long‐term isolation and genetic differentiation. These results highlight the complex nature of diversification in archipelagos: marine barriers, changes in connectivity due to sea level change, and climate‐induced refugia acted in concert to produce great species diversity and endemism in the Philippines.

Phylogeny and biogeography of the Asian trogons (Aves: Trogoniformes) inferred from nuclear and mitochondrial DNA sequences.

We present the first species-level molecular phylogenetic hypothesis for the Asian trogons, using DNA sequences of multiple mitochondrial and nuclear loci, and Bayesian and maximum likelihood tree reconstruction methods. The two genera of Asian trogons, Harpactes and Apalharpactes, are distantly related to each other. Within the widespread Southeast Asian genus Harpactes, we recovered three species groups: (1) H. oreskios; (2) H. orrhophaeus and H. duvaucelii; and (3) a clade of the seven large-bodied species. Short internal branch lengths link species in the large-bodied group, suggesting rapid diversification. Apalharpactes, which is currently restricted to the montane forests of Sumatra and Java, appears to be a relictual lineage distantly related to all other trogons. Bayesian and maximum likelihood analyses indicate Apalharpactes is sister to the African genus Apaloderma, although this result was not strongly supported. Overall, the extant Asian trogon species appear to have diversified prior to the Pleistocene, based on large pair-wise mitochondrial divergences between taxa.

Distribution, Behavior, and Conservation Status of the Rufous Twistwing (Cnipodectes superrufus)

Abstract The Rufous Twistwing (Cnipodectes superrufus), a newly described Amazonian tyrant-flycatcher, is known from five specimens and five localities in Cuzco and western Madre de Dios departments, Peru. We report three additional specimens and eight new localities extending the known range of the species east across Dpto. Madre de Dios, Peru, into Dpto. Pando, Bolivia, and Acre State, Brazil. The new localities increase the distribution from ∼3,400 to ∼89,000 km2. We collected biometric data from five individuals, made behavioral observations in the field, and recorded three separate types of vocalizations, two of which (including the song) were previously unknown. We provide quantitative description of these vocalizations, consider their function, and compare them with vocalizations of the only known congener, the Brownish Twistwing (Cnipodectes subbrunneus). Unique vocal repertoires support the classification of these two forms as sister species. The Rufous Twistwing resembles the Brownish Twistwing in producing loud vocalizations from regular song posts and both species appear to have a polygamous mating system. We provide further evidence consistent with the hypothesis the Rufous Twistwing is a Guadua bamboo specialist and recommend that it be listed as Vulnerable on the IUCN Red List.

Phylogeography of the Robsonius Ground-Warblers (Passeriformes: Locustellidae) Reveals an Undescribed Species from Northeastern Luzon, Philippines

Abstract. The Robsonius ground-warblers are forest birds endemic to the Luzon Island complex in the Philippine archipelago. Their systematic relationships have long remained ambiguous; until recently they were included in the timaliid genus Napothera. Two Robsonius species are currently recognized on the basis of plumage differences: R. rabori from northern Luzon in the Cordillera Central and the northern Sierra Madre, and R. sorsogonensis from southern Luzon and Catanduanes Island. Recent specimen collections, including the first adult specimen from the Cordillera Central, establish plumage differences between populations of R. rabori in the Cordillera Central and Sierra Madre and reveal a third diagnosable population within Luzon. These differences have gone unnoticed because R. rabori (sensu stricto) had been known only from the juvenile holotype. Molecular phylogenetic data further support the hypothesis that three highly divergent taxa occur across the Luzon Island complex: Robsonius rabori is known only from the northern Cordillera Central in Ilocos Norte; an undescribed taxon (formerly included in R. rabori) occurs in the northern Sierra Madre in Cagayan, Isabela, Aurora, and Nueva Vizcaya provinces; and R. sorsogonensis occurs in southern Luzon (Bulacan and Laguna provinces), the Bicol Peninsula, and on Catanduanes Island. The existence of three putatively allopatric species within the Luzon island complex highlights the role of in situ diversification in island systems, and brings attention to the need for forest conservation to protect geographically restricted populations throughout the Luzon Island complex.

Sorting out relationships among the grouse and ptarmigan using intron, mitochondrial, and ultra-conserved element sequences

The Holarctic phasianid clade of the grouse and ptarmigan has received substantial attention in areas such as evolution of mating systems, display behavior, and population ecology related to their conservation and management as wild game species. There are multiple molecular phylogenetic studies that focus on grouse and ptarmigan. In spite of this, there is little consensus regarding historical relationships, particularly among genera, which has led to unstable and partial taxonomic revisions. We estimated the phylogeny of all currently recognized species using a combination of novel data from seven nuclear loci (largely intron sequences) and published data from one additional autosomal locus, two W-linked loci, and four mitochondrial regions. To explore relationships among genera and assess paraphyly of one genus more rigorously, we then added over 3000 ultra-conserved element (UCE) loci (over 1.7million bp) gathered using Illumina sequencing. The UCE topology agreed with that of the combined nuclear intron and previously published sequence data with 100% bootstrap support for all relationships. These data strongly support previous studies separating Bonasa from Tetrastes and Dendragapus from Falcipennis. However, the placement of Lagopus differed from previous studies, and we found no support for Falcipennis monophyly. Biogeographic analysis suggests that the ancestors of grouse and ptarmigan were distributed in the New World and subsequently underwent at least four dispersal events between the Old and New Worlds. Divergence time estimates from maternally-inherited and autosomal markers show stark differences across this clade, with divergence time estimates from maternally-inherited markers being nearly half that of the autosomal markers at some nodes, and nearly twice that at other nodes.

A New Species of Scytalopus Tapaculo (Aves: Passeriformes: Rhinocryptidae) from the Andes of Central Peru

Abstract We describe a new species of Scytalopus tapaculo (Aves: Passeriformes: Rhinocryptidae) from the temperate humid montane forests (2,400–3,200 m) of Junín Department, Peru. This species has a unique song that differs strikingly from that of any known Scytalopus species, consisting of a rapidly repeated series of ascending phrases. Phenotypically, the new species is uniformly blackish in color and small-to-medium in size, most similar to members of the allopatric S. latrans complex. At least six species of Scytalopus occur along an elevational gradient on the eastern slopes of the Andes in Junín; in the vicinity of the type locality, the new species replaces S. femoralis at 2,400–2,500 m, and is replaced by S. acutirostris at 2,900–3,200 m. Throughout its elevational range, the new species is broadly syntopic with the larger S. macropus. This species is currently known from a single river drainage; although it probably occurs more broadly, it is likely a range-restricted species endemic to central Peru.

Phylogeny and biogeography of Ficedula flycatchers (Aves: Muscicapidae): novel results from fresh source material.

The avian genus Ficedula has been a model system for studying speciation, genomics, biogeography, and the evolution of migratory behavior. However, no multi-locus molecular phylogenetic hypothesis exists for the genus. We expanded taxon and character sampling over previous studies and produced a robust hypothesis of relationships for the genus. Many previous findings, such as the inclusion of Muscicapella and exclusion of Ficedula monileger from the genus, were verified, but many relationships differed compared to previous work. Some of the differences were due to increased sampling, but others were due to problematic sequence data produced from DNA extracted from historical museum specimens. The new phylogenetic hypothesis resulted in a simpler biogeographic scenario with fewer transitions between regions and fewer transitions between seasonally migratory and resident character states. Notably, all species endemic to the Philippines and Wallacea formed a clade, which included Ficedula dumetoria of the Sunda Shelf and Lesser Sundas. In addition, Ficedula hyperythra was not monophyletic; samples from Philippine populations formed a clade distantly related to a clade that comprised all other sampled populations.