Allison J. Shultz

Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds

Thraupidae is the second largest family of birds and represents about 4% of all avian species and 12% of the Neotropical avifauna. Species in this family display a wide range of plumage colors and patterns, foraging behaviors, vocalizations, ecotypes, and habitat preferences. The lack of a complete phylogeny for tanagers has hindered the study of this evolutionary diversity. Here, we present a comprehensive, species-level phylogeny for tanagers using six molecular markers. Our analyses identified 13 major clades of tanagers that we designate as subfamilies. In addition, two species are recognized as distinct branches on the tanager tree. Our topologies disagree in many places with previous estimates of relationships within tanagers, and many long-recognized genera are not monophyletic in our analyses. Our trees identify several cases of convergent evolution in plumage ornaments and bill morphology, and two cases of social mimicry. The phylogeny produced by this study provides a robust framework for studying macroevolutionary patterns and character evolution. We use our new phylogeny to study diversification processes, and find that tanagers show a background model of exponentially declining diversification rates. Thus, the evolution of tanagers began with an initial burst of diversification followed by a rate slowdown. In addition to this background model, two later, clade-specific rate shifts are supported, one increase for Darwins finches and another increase for some species of Sporophila. The rate of diversification within these two groups is exceptional, even when compared to the overall rapid rate of diversification found within tanagers. This study provides the first robust assessment of diversification rates for the Darwins finches in the context of the larger group within which they evolved.

Widespread Cryptic Dichromatism and Ultraviolet Reflectance in the Largest Radiation of Neotropical Songbirds: Implications of Accounting for Avian Vision in the Study of Plumage Evolution

ABSTRACT. Avian coloration has played a central role in the study of sexual selection and other aspects of animal behavior. However, only recently have analyses of avian coloration been able to incorporate avian visual abilities. Although several studies have broadly sampled species for evidence of plumage coloration visible to birds but invisible to humans, few studies have quantified these data for all species in a single taxonomic group. We quantify ultraviolet (UV) plumage reflectance and document cryptic sexual dichromatism in the largest radiation of Neotropical songbirds, the cardinals and tanagers. Ultraviolet reflectance was common in the patches measured, with almost half of the species reflecting >20% of light in the UV range in at least one patch. High UV-reflecting patches, including 73 of the 91 patches that were found to be primarily UV colored, belonged to species in either Passerina or 2 of 13 major clades of tanagers. This indicates that high UV reflectance is not randomly distributed across the phytogeny. Sexual dichromatism was much more widespread in the group than previously thought. From a human visual perspective, about half the species in the group are sexually dichromatic; but from an avian visual perspective, 97% of species are dichromatic. We compared the implications of using human-perceived versus avian-perceived sexual dichromatism by mapping these traits onto tanager phytogenies. Quantifying dichromatism using an avian visual model provided a more accurate and detailed history of plumage coloration change across evolutionary history.

Elaborate visual and acoustic signals evolve independently in a large, phenotypically diverse radiation of songbirds.

The concept of a macroevolutionary trade-off among sexual signals has a storied history in evolutionary biology. Theory predicts that if multiple sexual signals are costly for males to produce or maintain and females prefer a single, sexually selected trait, then an inverse correlation between sexual signal elaborations is expected among species. However, empirical evidence for what has been termed the ‘transfer hypothesis’ is mixed, which may reflect different selective pressures among lineages, evolutionary covariates or methodological differences among studies. Here, we examine interspecific correlations between song and plumage elaboration in a phenotypically diverse, widespread radiation of songbirds, the tanagers. The tanagers (Thraupidae) are the largest family of songbirds, representing nearly 10% of all songbirds. We assess variation in song and plumage elaboration across 301 species, representing the largest scale comparative study of multimodal sexual signalling to date. We consider whether evolutionary covariates, including habitat, structural and carotenoid-based coloration, and subfamily groupings influence the relationship between song and plumage elaboration. We find that song and plumage elaboration are uncorrelated when considering all tanagers, although the relationship between song and plumage complexity varies among subfamilies. Taken together, we find that elaborate visual and vocal sexual signals evolve independently among tanagers.

Plumage evolution in relation to light environment in a novel clade of Neotropical tanagers

Molecular phylogenetic analyses have greatly changed Neotropical avian systematics in the past couple of decades. These new phylogenies provide the necessary framework to study the ecology and natural history of species in the region in an evolutionary context. This study addresses the systematics of Poospiza, Compsospiza, Hemispingus, Thlypopsis, and eight monotypic genera, which form a strongly supported and novel clade within the tanagers. We find Poospiza, Hemispingus, and Thlypopsis to be polyphyletic, confirm or reject relationships proposed based on morphology and life history, and describe novel relationships among these and the monotypic genera. The diversity of plumage, habitat, and geography throughout the clade allows us to test hypotheses of plumage evolution in relation to light environment. We find that overall plumage brightness best fits a model that includes selective regimes based on open versus closed habitats and foraging strata, while plumage measures describing color diversity and chroma best fit a model that only includes selective regimes based on open and closed habitats.

Next-generation sequencing and the expanding domain of phylogeography

Abstract. Phylogeography is experiencing a revolution brought on by next-generation sequencing methods. A historical survey of the phylogeographic literature suggests that phylogeography typically incorporates new questions, expanding on its classical domain, when new technologies offer novel or increased numbers of molecular markers. A variety of methods for subsampling genomic variation, including restriction site associated DNA sequencing (Rad-seq) and other next generation approaches, are proving exceptionally useful in helping to define major phylogeographic lineages within species as well as details of historical demography. Next-generation methods are also blurring the edges of phylogeography and related fields such as association mapping of loci under selection, and the emerging paradigm is one of simultaneously inferring both population history across geography and genomic targets of selection. However, recent examples, including some from our lab on Anolis lizards and songbirds, suggest that genome subsampling methods, while extremely powerful for the classical goals of phylogeography, may fail to allow phylogeography to fully achieve the goals of this new, expanded domain. Specifically, if genome-wide linkage disequilibrium is low, as is the case in many species with large population sizes, most genome subsampling methods will not sample densely enough to detect selected variants, or variants closely linked to them. We suggest that whole-genome resequencing methods will be essential for allowing phylogeographers to robustly identify loci involved in phenotypic divergence and speciation, while at the same time allowing free choice of molecular markers and further resolution of the demographic history of species.

A Century of Avian Community Turnover in an Urban Green Space in Northern California

Abstract. Over long time periods, urbanization is expected to have a negative effect on species diversity. Predicted effects generally follow one of three competing paradigms: diversity decay, homogenization, or community-composition turnover. However, it has been hypothesized that urban green spaces may provide a means by which urban areas can maintain or increase their species diversity over time. We used surveys conducted in 1913–18,1938– 39, and 2006–07 on the campus of the University of California, Berkeley, to evaluate how an avian community has changed over time in the context of urban growth. In each of the three periods the community differed greatly, yet we found no evidence for a decline in species or functional diversity. Despite the birds of the 1913–18 community having a greater affinity for native habitats than birds of later periods, we found no further evidence that specialists were being replaced by generalists. Of the three paradigms, our results strongly supported community-composition turnover. Parsimoniously, the habitat preferences of groups of species that changed over time were concordant with known changes in landscaping. While urbanization often does result in decreased biodiversity, our results provide an example of how an urban green space can mitigate and potentially reverse this trend within the context of dynamic community change. Our results are concordant with the view that urban green spaces can maintain original bird communities and disturbance-sensitive species can reestablish themselves given appropriate conditions.

Iridescent colour production in hairs of blind golden moles (Chrysochloridae)

Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.

Morphological and genomic comparisons of Hawaiian and Japanese Black-footed Albatrosses (Phoebastria nigripes) using double digest RADseq: implications for conservation.

Evaluating the genetic and demographic independence of populations of threatened species is important for determining appropriate conservation measures, but different technologies can yield different conclusions. Despite multiple studies, the taxonomic status and extent of gene flow between the main breeding populations of Black‐footed Albatross (Phoebastria nigripes), a Near‐Threatened philopatric seabird, are still controversial. Here, we employ double digest RADseq to quantify the extent of genomewide divergence and gene flow in this species. Our genomewide data set of 9760 loci containing 3455 single nucleotide polymorphisms yielded estimates of genetic diversity and gene flow that were generally robust across seven different filtering and sampling protocols and suggest a low level of genomic variation (θ per site = ~0.00002–0.00028), with estimates of effective population size (Ne = ~500–15 881) falling far below current census size. Genetic differentiation was small but detectable between Japan and Hawaii (FST ≈ 0.038–0.049), with no FST outliers. Additionally, using museum specimens, we found that effect sizes of morphological differences by sex or population rarely exceeded 4%. These patterns suggest that the Hawaiian and Japanese populations exhibit small but significant differences and should be considered separate management units, although the evolutionary and adaptive consequences of this differentiation remain to be identified.

SNPs across time and space: population genomic signatures of founder events and epizootics in the House Finch (Haemorhous mexicanus)

Abstract Identifying genomic signatures of natural selection can be challenging against a background of demographic changes such as bottlenecks and population expansions. Here, we disentangle the effects of demography from selection in the House Finch (Haemorhous mexicanus) using samples collected before and after a pathogen‐induced selection event. Using ddRADseq, we genotyped over 18,000 SNPs across the genome in native pre‐epizootic western US birds, introduced birds from Hawaii and the eastern United States, post‐epizootic eastern birds, and western birds sampled across a similar time span. We found 14% and 7% reductions in nucleotide diversity, respectively, in Hawaiian and pre‐epizootic eastern birds relative to pre‐epizootic western birds, as well as elevated levels of linkage disequilibrium and other signatures of founder events. Despite finding numerous significant frequency shifts (outlier loci) between pre‐epizootic native and introduced populations, we found no signal of reduced genetic diversity, elevated linkage disequilibrium, or outlier loci as a result of the epizootic. Simulations demonstrate that the proportion of outliers associated with founder events could be explained by genetic drift. This rare view of genetic evolution across time in an invasive species provides direct evidence that demographic shifts like founder events have genetic consequences more widespread across the genome than natural selection.

The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae)

Males and females can be under different evolutionary pressures if sexual and natural selection is differentially operating in each sex. As a result, many species have evolved sexual dichromatism, or differences in coloration between sexes. Although sexual dichromatism is often used as an index of the magnitude of sexual selection, sexual dichromatism is a composite trait. Here, we examine the evolution of sexual dichromatism in one of the largest and most ecologically diverse families of birds, the tanagers, using the avian visual perspective and a species‐level phylogeny. Our results demonstrate that the evolutionary decreases of sexual dichromatism are more often associated with larger and more frequent changes in male plumage coloration, and evolutionary increases are not more often associated with larger changes in either sex. Furthermore, we show that the crown and ventral plumage regions are correlated with sexual dichromatism in males, and that only male plumage complexity is positively correlated with sexual dichromatism. Finally, we demonstrate that light environment is important in shaping both plumage brilliance and complexity. By conducting a multilevel analysis of plumage evolution in males and females, we show that sexual dichromatism evolves via a mosaic of sexual and natural selection in both sexes.