Joseph D. Manthey

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.

RELATIONSHIP OF GENETIC DIVERSITY AND NICHE CENTRALITY: A SURVEY AND ANALYSIS

The distribution of genetic diversity within and among populations in relation to species’ geographic ranges is important to understanding processes of evolution, speciation, and biogeography. One hypothesis predicts that natural populations at geographic range margins will have lower genetic diversity relative to those located centrally in species’ distributions owing to a link between geographic and environmental marginality; alternatively, genetic variation may be unrelated with geographic marginality via decoupling of geographic and environmental marginality. We investigate the predictivity of geographic patterns of genetic variation based on geographic and environmental marginality using published genetic diversity data for 40 species (insects, plants, birds, mammals, worms). Only about half of species showed positive relationships between geographic and environmental marginality. Three analyses (sign test, multiple linear regression, and meta‐analysis of correlation effect sizes) showed a negative relationship between genetic diversity and distance to environmental niche centroid, but no consistent relationship of genetic diversity with distance to geographic range center.

Comparison of Target-Capture and Restriction-Site Associated DNA Sequencing for Phylogenomics: A Test in Cardinalid Tanagers (Aves, Genus: Piranga)

Restriction-site associated DNA sequencing (RAD-seq) and target capture of specific genomic regions, such as ultraconserved elements (UCEs), are emerging as two of the most popular methods for phylogenomics using reduced-representation genomic data sets. These two methods were designed to target different evolutionary timescales: RAD-seq was designed for population-genomic level questions and UCEs for deeper phylogenetics. The utility of both data sets to infer phylogenies across a variety of taxonomic levels has not been adequately compared within the same taxonomic system. Additionally, the effects of uninformative gene trees on species tree analyses (for target capture data) have not been explored. Here, we utilize RAD-seq and UCE data to infer a phylogeny of the bird genus Piranga The group has a range of divergence dates (0.5-6 myr), contains 11 recognized species, and lacks a resolved phylogeny. We compared two species tree methods for the RAD-seq data and six species tree methods for the UCE data. Additionally, in the UCE data, we analyzed a complete matrix as well as data sets with only highly informative loci. A complete matrix of 189 UCE loci with 10 or more parsimony informative (PI) sites, and an approximately 80% complete matrix of 1128 PI single-nucleotide polymorphisms (SNPs) (from RAD-seq) yield the same fully resolved phylogeny of Piranga We inferred non-monophyletic relationships of Piranga lutea individuals, with all other a priori species identified as monophyletic. Finally, we found that species tree analyses that included predominantly uninformative gene trees provided strong support for different topologies, with consistent phylogenetic results when limiting species tree analyses to highly informative loci or only using less informative loci with concatenation or methods meant for SNPs alone.

Isolation by environment in White-breasted Nuthatches (Sitta carolinensis) of the Madrean Archipelago sky islands: a landscape genomics approach.

Understanding landscape processes driving patterns of population genetic differentiation and diversity has been a long‐standing focus of ecology and evolutionary biology. Gene flow may be reduced by historical, ecological or geographic factors, resulting in patterns of isolation by distance (IBD) or isolation by environment (IBE). Although IBE has been found in many natural systems, most studies investigating patterns of IBD and IBE in nature have used anonymous neutral genetic markers, precluding inference of selection mechanisms or identification of genes potentially under selection. Using landscape genomics, the simultaneous study of genomic and ecological landscapes, we investigated the processes driving population genetic patterns of White‐breasted Nuthatches (Sitta carolinensis) in sky islands (montane forest habitat islands) of the Madrean Archipelago. Using more than 4000 single nucleotide polymorphisms and multiple tests to investigate the relationship between genetic differentiation and geographic or ecological distance, we identified IBE, and a lack of IBD, among sky island populations of S. carolinensis. Using three tests to identify selection, we found 79 loci putatively under selection; of these, seven matched CDS regions in the Zebra Finch. The loci under selection were highly associated with climate extremes (maximum temperature of warmest month and minimum precipitation of driest month). These results provide evidence for IBE – disentangled from IBD – in sky island vertebrates and identify potential adaptive genetic variation.

A genome wide assessment of stages of elevational parapatry in Bornean passerine birds reveals no introgression: implications for processes and patterns of speciation

Topographically complex regions often contain the close juxtaposition of closely related species along elevational gradients. The evolutionary causes of these elevational replacements, and thus the origin and maintenance of a large portion of species diversity along elevational gradients, are usually unclear because ecological differentiation along a gradient or secondary contact following allopatric diversification can produce the same pattern. We used reduced representation genomic sequencing to assess genetic relationships and gene flow between three parapatric pairs of closely related songbird taxa (Arachnothera spiderhunters, Chloropsis leafbirds, and Enicurus forktails) along an elevational gradient in Borneo. Each taxon pair presents a different elevational range distribution across the island, yet results were uniform: little or no gene flow was detected in any pairwise comparisons. These results are congruent with an allopatric “species-pump” model for generation of species diversity and elevational parapatry of congeners on Borneo, rather than in situ generation of species by “ecological speciation” along an elevational gradient.

A genomic investigation of the putative contact zone between divergent Brown Creeper (Certhia americana) lineages: chromosomal patterns of genetic differentiation.

Sky islands, or montane forest separated by different lowland habitats, are highly fragmented regions that potentially limit gene flow between isolated populations. In the sky islands of the Madrean Archipelago (Arizona, USA), various taxa display different phylogeographic patterns, from unrestricted gene flow among sky islands to complex patterns with multiple distinct lineages. Using genomic-level approaches allows the investigation of differential patterns of gene flow, selection, and genetic differentiation among chromosomes and specific genomic regions between sky island populations. Here, we used thousands of SNPs to investigate the putative contact zone of divergent Brown Creeper (Certhia americana) lineages in the Madrean Archipelago sky islands. We found the two lineages to be completely allopatric (during the breeding season) with a lack of hybridization and gene flow between lineages and no genetic structure among sky islands within lineages. Additionally, the two lineages inhabit different climatic and ecosystem conditions and have many local primary song dialects in the southern Arizona mountain ranges. We identified a positive relationship between genetic differentiation and chromosome size, but the sex chromosome (Z) was not found to be an outlier. Differential patterns of genetic differentiation per chromosome may be explained by genetic drift--possibly in conjunction with non-random mating and non-random gene flow--due to variance in recombination rates among chromosomes.

Conservation genomics of the silktail (Aves: Lamprolia victoriae) suggests the need for increased protection of native forest on the Natewa Peninsula, Fiji

Effective conservation relies on accurate taxonomy, because we cannot protect what we do not know. Species limits among phenotypically differentiated and allopatrically distributed populations on Southwest Pacific islands are poorly understood. This likely has led to an underestimate of species richness in the Southwest Pacific, and, consequently, a biased application of conservation effort. The silktail Lamprolia victoriae is a bird species endemic to Fiji. Two subspecies are known from Vanua Levu and Taveuni Islands, but uncertainty remains whether they should be considered one or two species. If the latter, increased conservation effort is warranted to protect forest habitat where isolated populations occur only on the Natewa Peninsula. Here, we address this question by examining 8859 single nucleotide polymorphisms produced by restriction-site associated DNA sequencing. We find that the silktail is best considered two species, due to high genetic differentiation and low gene flow between the two subspecies. These differences match known phenotypic differences (size and plumage), as well as allopatric island distributions. We suggest that the silktail be used as an icon for conservation efforts of the heavily degraded forest habitats on the Natewa Peninsula. Finally, we reassess the divergence age estimates of Lamprolia and its relatives, Chaetorhynchus and Rhipidura, in light of new phylogenomic evidence from oscine passerines.

Genomic insights into hybridization in a localized region of sympatry between pewee sister species (Contopus sordidulus × C. virens) and their chromosomal patterns of differentiation

BackgroundThe Great Plains of the United States includes a large number of hybrid and contact zones between bird species. The amount of gene flow between sister species in these zones ranges from very rare hybridization events to widespread and prevalent introgression. Some of these avian systems have been studied extensively, while others have been indeterminate of whether hybridization exists in areas of sympatry. Using genomic-level approaches allows investigation of genomic patterns of hybridization and gene flow between species—or lack thereof.MethodsWe investigated a narrow zone of sympatry in Nebraska, USA between pewee species (Contopus sordidulus and C. virens), for which no hybridization has been confirmed. We used thousands of single nucleotide polymorphisms to identify potential hybridization and investigate genomic patterns of differentiation between these two species.ResultsWe found evidence of multiple hybrid individuals in the contact zone. Little genomic variation was fixed between species, but a large proportion had differentiated allele frequencies between species. There was a positive relationship between genetic differentiation and chromosome size.ConclusionsWe provided the first conclusive evidence of hybridization between C.sordidulus and C. virens, in a region where secondary contact likely occurred due to human disturbance and habitat modification. The genomic patterns of differentiation affirm that these species split in the relatively recent past. Finally, the relationship of chromosome size and genetic differentiation may have resulted from differential rates of chromosomal recombination in songbirds and genetic differentiation between species largely due to genetic drift (possibly in concert with selection).