Specimen collection is essential for modern science.

Natural history museums are vital repositories of specimens, samples and data that inform about the natural world; this Formal Comment revisits a Perspective that advocated for the adoption of compassionate collection practices, querying whether it will ever be possible to completely do away with whole animal specimen collection.

Sampling affects population genetic inference: A case study of the Allen's (Selasphorus sasin) and rufous hummingbird (Selasphorus rufus).

Gene flow can affect evolutionary inference when species are undersampled. Here, we evaluate the effects of gene flow and geographic sampling on demographic inference of 2 hummingbirds that hybridize, Allen's hummingbird (Selasphorus sasin) and rufous hummingbird (Selasphorus rufus). Using whole-genome data and extensive geographic sampling, we find widespread connectivity, with introgression far beyond the Allen's × rufous hybrid zone, although the Z chromosome resists introgression beyond the hybrid zone. We test alternative hypotheses of speciation history of Allen's, rufous, and Calliope (S. calliope) hummingbird and find that rufous hummingbird is the sister taxon to Allen's hummingbird, and Calliope hummingbird is the outgroup. A model treating the 2 subspecies of Allen's hummingbird as a single panmictic population fit observed genetic data better than models treating the subspecies as distinct populations, in contrast to morphological and behavioral differences and analyses of spatial population structure. With additional sampling, our study builds upon recent studies that came to conflicting conclusions regarding the evolutionary histories of these 2 species. Our results stress the importance of thorough geographic sampling when assessing demographic history in the presence of gene flow.

Widespread convergent morphological evolution within the largest family of songbirds.

Although convergence is a common evolutionary phenomenon, few studies have quantified its prevalence across a large, densely sampled clade. Large-scale phylogenies and the advent of novel computational methods facilitate more robust identification of convergent events and their statistical significance. The tanagers (Aves: Thraupidae), the largest family of songbirds, offer an excellent opportunity to study the extent of phenotypic convergence in response to similar ecological pressures on a continental scale. To investigate convergence in the group, we used the largest phylogenetic and multivariate morphological dataset to date for the clade. First, we used phylogenetic comparative analyses to show a correlation between diet and aspects of bill shape. We then investigated our dataset for the presence and magnitude of convergent events and assessed significance through simulations and modeling analyses. Overall, we found that around half (45.3%) of species and clades we tested have converged in morphological space more than would be expected by chance alone. Our study shows that across Thraupidae, various bill shapes have evolved convergently to fill multiple distinct sections of ecological niche space, reflecting a signal of ecological opportunity and structural constraints.

The population genetics of nonmigratory Allen's Hummingbird (Selasphorus sasin sedentarius) following a recent mainland colonization.

Allen's Hummingbird comprises two subspecies, one migratory (Selasphorus sasin sasin) and one nonmigratory (S. s. sedentarius). The nonmigratory subspecies, previously endemic to the California Channel Islands, apparently colonized the California mainland on the Palos Verdes Peninsula some time before 1970 and now breeds throughout coastal southern California. We sequenced and compared populations of mainland nonmigratory Allen's Hummingbird to Channel Island populations from Santa Catalina, San Clemente, and Santa Cruz Island. We found no evidence of founder effects on the mainland population. Values of nucleotide diversity on the mainland were higher than on the Channel Islands. There were low levels of divergence between the Channel Islands and the mainland, and Santa Cruz Island was the most genetically distinct. Ecological niche models showed that rainfall and temperature variables on the Channel Islands are similar in the Los Angeles basin and predicted continued expansion of nonmigratory Allen's Hummingbird north along the coast and inland. We also reviewed previous genetic studies of vertebrate species found on the Channel Islands and mainland and showed that broad conclusions regarding island-mainland patterns remain elusive. Challenges include the idiosyncratic nature of colonization itself as well as the lack of a comprehensive approach that incorporates similar markers and sampling strategies across taxa, which, within the context of a comparative study of island-mainland relationships, may lead to inconsistent results.

Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds.

Although evolutionary theory predicts an association between the evolution of elaborate ornamentation and speciation, empirical evidence for links between speciation and ornament evolution has been mixed. In birds, the evolution of increasingly complex and colorful plumage may promote speciation by introducing prezygotic mating barriers. However, overall changes in color complexity, including both increases and decreases, may also promote speciation by altering the sexual signals that mediate reproductive choices. Here, we examine the relationship between complex plumage and speciation rates in the largest family of songbirds, the tanagers (Thraupidae). First, we test whether species with more complex plumage coloration are associated with higher speciation rates and find no correlation. We then test whether rates of male or female plumage color complexity evolution are correlated with speciation rates. We find that elevated rates of plumage complexity evolution are associated with higher speciation rates, regardless of sex and whether species are evolving more complex or less complex ornamentation. These results extend to whole-plumage color complexity and regions important in signaling (crown and throat) but not nonsignaling regions (back and wingtip). Our results suggest that the extent of change in plumage traits, rather than overall values of plumage complexity, may play a role in speciation.

Two overlooked generic synonyms in the Thraupidae (Aves: Passeriformes).

In a revision of the generic classification of the tanagers, Burns et al. (2016) proposed the name Islerothraupis with type species Tanagra cristata Linnaeus, 1766 (long known as Tachyphonus cristatus); however, they overlooked a previous designation of that species as the type of a genus. In 1821, Feliks Pawel Jarocki, in the second volume of Zoologiia czyli Zwiérzetopismo Ogólne podlug Naynowszego Systematu ulozone ("Zoology, or general natural history account according to the newest arranged system"), page 133, specified Tanagra cristata as the type of a proposed subgenus Loriotus. The original text in Polish is available at the website www.rcin.org.pl, the Digital Repository of Scientific Institutes, which has made a wide diversity of scholarship in Polish available over the Internet. The original description of Loriotus, in parallel with other names Jarocki introduced in his Zoologiia, is minimal: "Dziób ostro konczysty, cokolwiek zgiety. Zuchwy sczeki spodniey przy nasadzie bardzo malo zgrubiale." (Bill ending in a point, somewhat curved. Lower mandible slightly thickened at base.).

Mitochondrial genomes of the bird genus Piranga: rates of sequence evolution, and discordance between mitochondrial and nuclear markers.

We report the characteristics of the mitochondrial genomes of 22 individuals in the bird genus Piranga, including all currently recognized species in the genus (n = 11). Elements follow the standard avian mitogenome series, including two ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, 13 protein coding genes, and the mitochondrial control region. Excluding tRNA sequences, sequence divergence rate was lowest in rRNA genes and highest in genes encoding NADH (specifically ND1, ND2, ND3) and the control region. Gene trees assembled from 16 elements (non-tRNAs) varied greatly in topological concordance compared to the recognized species tree (based on thousands of nuclear loci), with no one gene tree precisely recovering all relationships in the genus. We also investigated patterns of concordance between the mitogenome tree and the nuclear species tree and found some discrepancies. Across non-tRNA gene trees (n = 16), the species tree topology was recovered by as few as three elements at a particular node and complete concordance (i.e. 16/16 gene trees matched the species tree topology) was recovered at only one node. We found mitochondrial gene regions that are often used in vertebrate systematics (e.g. CytB, ND2) recovered nearly the exact same topology as the nuclear species tree topology.

Contrasting impacts of competition on ecological and social trait evolution in songbirds.

Competition between closely related species has long been viewed as a powerful selective force that drives trait diversification, thereby generating phenotypic diversity over macroevolutionary timescales. However, although the impact of interspecific competition has been documented in a handful of iconic insular radiations, most previous studies have focused on traits involved in resource use, and few have examined the role of competition across large, continental radiations. Thus, the extent to which broad-scale patterns of phenotypic diversity are shaped by competition remain largely unclear, particularly for social traits. Here, we estimate the effect of competition between interacting lineages by applying new phylogenetic models that account for such interactions to an exceptionally complete dataset of resource-use traits and social signaling traits for the entire radiation of tanagers (Aves, Thraupidae), the largest family of songbirds. We find that interspecific competition strongly influences the evolution of traits involved in resource use, with a weaker effect on plumage signals, and very little effect on song. Our results provide compelling evidence that interspecific exploitative competition contributes to ecological trait diversification among coexisting species, even in a large continental radiation. In comparison, signal traits mediating mate choice and social competition seem to diversify under different evolutionary models, including rapid diversification in the allopatric stage of speciation.

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.

Song evolution, speciation, and vocal learning in passerine birds.

Phenotypic divergence can promote reproductive isolation and speciation, suggesting a possible link between rates of phenotypic evolution and the tempo of speciation at multiple evolutionary scales. To date, most macroevolutionary studies of diversification have focused on morphological traits, whereas behavioral traits─including vocal signals─are rarely considered. Thus, although behavioral traits often mediate mate choice and gene flow, we have a limited understanding of how behavioral evolution contributes to diversification. Furthermore, the developmental mode by which behavioral traits are acquired may affect rates of behavioral evolution, although this hypothesis is seldom tested in a phylogenetic framework. Here, we examine evidence for rate shifts in vocal evolution and speciation across two major radiations of codistributed passerines: one oscine clade with learned songs (Thraupidae) and one suboscine clade with innate songs (Furnariidae). We find that evolutionary bursts in rates of speciation and song evolution are coincident in both thraupids and furnariids. Further, overall rates of vocal evolution are higher among taxa with learned rather than innate songs. Taken together, these findings suggest an association between macroevolutionary bursts in speciation and vocal evolution, and that the tempo of behavioral evolution can be influenced by variation in developmental modes among lineages.

A genus-level classification of the family Thraupidae (Class Aves: Order Passeriformes).

The tanagers (Thraupidae) are a major component of the Neotropical avifauna, and vary in plumage colors, behaviors, morphologies, and ecologies. Globally, they represent nearly 4% of all avian species and are the largest family of songbirds. However, many currently used tanager genera are not monophyletic, based on analyses of molecular data that have accumulated over the past 25 years. Current genus-level classifications of tanagers have not been revised according to newly documented relationships of tanagers for various reasons: 1) the lack of a comprehensive phylogeny, 2) reluctance to lump existing genera into larger groups, and 3) the lack of available names for newly defined smaller groups. Here, we present two alternative classifications based on a newly published comprehensive phylogeny of tanagers. One of these classifications uses existing generic names, but defines them broadly. The other, which we advocate and follow here, provides new generic names for more narrowly defined groups. Under the latter, we propose eleven new genera (Asemospiza, Islerothraupis, Maschalethraupis, Chrysocorypha, Kleinothraupis, Castanozoster, Ephippiospingus, Chionodacryon, Pseudosaltator, Poecilostreptus, Stilpnia), and resurrect several generic names to form monophyletic taxa. Either of these classifications would allow taxonomic authorities to reconcile classification with current understanding of tanager phylogenetic relationships. Having a more phylogenetically accurate classification for tanagers will facilitate the study and conservation of this important Neotropical radiation of songbirds.

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.

Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds.

By employing a recently inferred phylogeny and museum occurrence records, we examine the relationship of ecological niche evolution to diversification in the largest family of songbirds, the tanagers (Thraupidae). We test whether differences in species numbers in the major clades of tanagers can be explained by differences in rate of climatic niche evolution. We develop a methodological pipeline to process and filter occurrence records. We find that, of the ecological variables examined, clade richness is higher in clades with higher climatic niche rate, and that this rate is also greater for clades that occupy a greater extent of climatic space. Additionally, we find that more speciose clades contain species with narrower niche breadths, suggesting that clades in which species are more successful at diversifying across climatic gradients have greater potential for speciation or are more buffered from the risk of extinction.

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.

A comprehensive multilocus assessment of sparrow (Aves: Passerellidae) relationships.

The New World sparrows (Emberizidae) are among the best known of songbird groups and have long-been recognized as one of the prominent components of the New World nine-primaried oscine assemblage. Despite receiving much attention from taxonomists over the years, and only recently using molecular methods, was a "core" sparrow clade established allowing the reconstruction of a phylogenetic hypothesis that includes the full sampling of sparrow species diversity. In this paper, we use mitochondrial DNA gene sequences from all 129 putative species of sparrow and four additional (nuclear) loci for a subset of these taxa to resolve both generic and species level relationships. Hypotheses derived from our mitochondrial (2184 base pairs) and nuclear (5705 base pairs) DNA data sets were generally in agreement with respect to clade constituency but differed somewhat with respect to among-clade relationships. Sparrow diversity is defined predominantly by eight well-supported clades that indicate a lack of monophyly for at least three currently recognized genera. Ammodramus is polyphyletic and requires the naming of two additional genera. Spizella is also polyphyletic with Tree Sparrow (Spizella arborea) as a taxonomic "outlier". Pselliophorus is embedded within a larger Atlapetes assemblage and should be merged with that group. This new hypothesis of sparrow relationships will form the basis for future comparative analyses of variation within songbirds.

Shared developmental programme strongly constrains beak shape diversity in songbirds.

The striking diversity of bird beak shapes is an outcome of natural selection, yet the relative importance of the limitations imposed by the process of beak development on generating such variation is unclear. Untangling these factors requires mapping developmental mechanisms over a phylogeny far exceeding model systems studied thus far. We address this issue with a comparative morphometric analysis of beak shape in a diverse group of songbirds. Here we show that the dynamics of the proliferative growth zone must follow restrictive rules to explain the observed variation, with beak diversity constrained to a three parameter family of shapes, parameterized by length, depth and the degree of shear. We experimentally verify these predictions by analysing cell proliferation in the developing embryonic beaks of the zebra finch. Our findings indicate that beak shape variability in many songbirds is strongly constrained by shared properties of the developmental programme controlling the growth zone.

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 Darwin's 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 Darwin's finches in the context of the larger group within which they evolved.

A comprehensive species-level molecular phylogeny of the New World blackbirds (Icteridae).

The New World blackbirds (Icteridae) are among the best known songbirds, serving as a model clade in comparative studies of morphological, ecological, and behavioral trait evolution. Despite wide interest in the group, as yet no analysis of blackbird relationships has achieved comprehensive species-level sampling or found robust support for most intergeneric relationships. Using mitochondrial gene sequences from all ∼108 currently recognized species and six additional distinct lineages, together with strategic sampling of four nuclear loci and whole mitochondrial genomes, we were able to resolve most relationships with high confidence. Our phylogeny is consistent with the strongly-supported results of past studies, but it also contains many novel inferences of relationship, including unexpected placement of some newly-sampled taxa, resolution of relationships among major clades within Icteridae, and resolution of genus-level relationships within the largest of those clades, the grackles and allies. We suggest taxonomic revisions based on our results, including restoration of Cacicus melanicterus to the monotypic Cassiculus, merging the monotypic Ocyalus and Clypicterus into Cacicus, restoration of Dives atroviolaceus to the monotypic Ptiloxena, and naming Curaeus forbesi to a new genus, Anumara. Our hypothesis of blackbird phylogeny provides a foundation for ongoing and future evolutionary analyses of the group.

The origin of finches on Tristan da Cunha and Gough Island, central South Atlantic ocean.

The Nesospiza finches of the Tristan da Cunha archipelago and Rowettia goughensis from Gough Island, 380 km distant, are both derived from tanager-finches (Thraupidae) that colonized the islands by crossing more than 3000 km of ocean from South America. Sequences from two mitochondrial and four nuclear genes indicate that the Patagonian bridled finches Melanodera are the closest relatives of the South Atlantic finches. Melanodera typically was sister to Rowettia, although some genes linked it more closely to Nesospiza. There was no evidence that Rowettia and Nesospiza are sister taxa, suggesting that the South Atlantic finches evolved from separate colonization events, as apparently was the case for moorhens Gallinula spp. at the two island groups. Genetic divergence between the two island finch genera thus provides an estimate of the maximum period of time they have been present at the islands, some 3-5 million years. A brief review of colonization histories suggests that island hopping by passerine birds is infrequent among islands more than 100-200 km apart.