Darío A. Lijtmaer

Probing Evolutionary Patterns in Neotropical Birds through DNA Barcodes

Background The Neotropical avifauna is more diverse than that of any other biogeographic region, but our understanding of patterns of regional divergence is limited. Critical examination of this issue is currently constrained by the limited genetic information available. This study begins to address this gap by assembling a library of mitochondrial COI sequences, or DNA barcodes, for Argentinian birds and comparing their patterns of genetic diversity to those of North American birds. Methodology and Principal Findings Five hundred Argentinian species were examined, making this the first major examination of DNA barcodes for South American birds. Our results indicate that most southern Neotropical bird species show deep sequence divergence from their nearest-neighbour, corroborating that the high diversity of this fauna is not based on an elevated incidence of young species radiations. Although species ages appear similar in temperate North and South American avifaunas, patterns of regional divergence are more complex in the Neotropics, suggesting that the high diversity of the Neotropical avifauna has been fueled by greater opportunities for regional divergence. Deep genetic splits were observed in at least 21 species, though distribution patterns of these lineages were variable. The lack of shared polymorphisms in species, even in species with less than 0.5M years of reproductive isolation, further suggests that selective sweeps could regularly excise ancestral mitochondrial polymorphisms. Conclusions These findings confirm the efficacy of species delimitation in birds via DNA barcodes, even when tested on a global scale. Further, they demonstrate how large libraries of a standardized gene region provide insight into evolutionary processes.

Rapid phenotypic evolution during incipient speciation in a continental avian radiation

Adaptive radiations have helped shape how we view animal speciation, particularly classic examples such as Darwins finches, Hawaiian fruitflies and African Great Lakes cichlids. These ‘island’ radiations are comparatively recent, making them particularly interesting because the mechanisms that caused diversification are still in motion. Here, we identify a new case of a recent bird radiation within a continentally distributed species group; the capuchino seedeaters comprise 11 Sporophila species originally described on the basis of differences in plumage colour and pattern in adult males. We use molecular data together with analyses of male plumage and vocalizations to understand species limits of the group. We find marked phenotypic variation despite lack of mitochondrial DNA monophyly and few differences in other putatively neutral nuclear markers. This finding is consistent with the group having undergone a recent radiation beginning in the Pleistocene, leaving genetic signatures of incomplete lineage sorting, introgressive hybridization and demographic expansions. We argue that this apparent uncoupling between neutral DNA homogeneity and phenotypic diversity is expected for a recent group within the framework of coalescent theory. Finally, we discuss how the ecology of open habitats in South America during the Pleistocene could have helped promote this unique and ongoing radiation.

DNA barcodes provide new evidence of a recent radiation in the genus Sporophila (Aves: Passeriformes)

The capuchinos are a group of birds in the genus Sporophila that has apparently radiated recently, as evidenced by their lack of mitochondrial genetic diversity. We obtained cytochrome c oxidase I (COI) sequences (or DNA barcodes) for the 11 species of the group and various outgroups. We compared the patterns of COI variability of the capuchinos with those of the largest barcode data set from neotropical birds currently available (500 species representing 51% of avian richness in Argentina), and subjected COI sequences to neighbour‐joining, maximum parsimony and Bayesian phylogenetic analyses as well as statistical parsimony network analysis. A clade within the capuchinos, the southern capuchinos, showed higher intraspecific and lower interspecific divergence than the remaining Argentine species. As most of the southern capuchinos shared COI haplotypes and pairwise distances within species were in many cases higher than distances between them, the phylogenetic affinities within the group remained unresolved. The observed genetic pattern is consistent with both incomplete lineage sorting and gene flow between species. The southern capuchinos constitute the only large group of species among the neotropical birds barcoded so far that are inseparable when using DNA barcodes, and one of few multispecies avian groups known to lack reciprocal monophyly. Extending the analysis to rapidly evolving nuclear and mitochondrial markers will be crucial to understanding this radiation. Apart from giving insights into the evolution of the capuchinos, this study shows how DNA barcoding can rapidly flag species or groups of species worthy of deeper study.

Paraphyly of Cinclodes fuscus (Aves: Passeriformes: Furnariidae): implications for taxonomy and biogeography.

The Andes are a hotspot of global avian diversity, but studies on the historical diversification of Andean birds remain relatively scarce. Evolutionary studies on avian lineages with Andean-Patagonian distributions have focused on reconstructing species-level phylogenies, whereas no detailed phylogeographic studies on widespread species have been conducted. Here, we describe phylogeographic patterns in the Bar-winged Cinclodes (Cinclodes fuscus), a widespread and common species of ovenbird (Furnariidae) that breeds from Tierra del Fuego to the northern Andes. Traditionally, C. fuscus has been considered a single species composed of nine subspecies, but its long and narrow range suggests the possibility of considerable genetic variation among populations. Sequences of two mitochondrial genes revealed three discrete and geographically coherent groups of C. fuscus, occupying the southern, central, and northern Andes. Surprisingly, phylogenetic analyses indicated that these groups were more closely related to other species of Cinclodes than to each other. Relationships of the southern and northern C. fuscus clades to other species of Cinclodes were straightforward; in combination with available information on plumage, behavioral, and vocal variation, this suggests that each should be recognized as a distinct biological species. The central Andean group was paraphyletic with respect to C. oustaleti, and relationships among these taxa and C. olrogi were poorly resolved. We suggest that the central Andean C. fuscus should also be considered a different species, pending new information to clarify species limits in this group. These new phylogenetic data, along with recently developed methods, allowed us to review the biogeography of the genus, confirming southern South America and the central Andes as important areas for the diversification of these birds.

Temporal stability and change in a microgeographical pattern of song variation in the rufous-collared sparrow

We studied the pattern of song variation in the rufous-collared sparrow, Zonotrichia capensis, in the 1987 and 2000 breeding seasons in a 7-km2 area covering open and closed habitats. We measured 14 quantitative song variables over a total of 390 individuals and found consistent differences between habitats in both years. In particular, songs of individuals from closed habitat sites had trills with longer trill intervals and lower frequencies than those of individuals from open habitats. This pattern of variation is interpreted as a song cline that correlates with the environmental gradient. Although this cline was stable in location and shape, it also showed several differences between years. The songs recorded during 2000 had trills with longer trill intervals and lower minimum frequencies than those recorded during 1987. Thus, this study is the first to directly document temporal changes in song variables in a Z. capensis population. This change would be expected if all the habitats studied were more closed in 2000 than in 1987, but we did not find obvious differences in habitat features between seasons. However, this modification of song structure is compatible with alternative explanations, such as subtle differences in habitat characteristics, changes in climatic variables, a delayed effect of a past modification of the environment and neutrality of the change.

Environmental Correlates of Song Structure in Forest Grosbeaks and Saltators

Abstract We compared the song structure of 19 species of forest grosbeaks and saltators based on the songs of 271 individuals recorded from Argentina to Canada, and analyzed their ecological correlates. On each spectrogram we measured eight temporal, frequency, and structural features of the song. Both a principal components analysis and a univariate analysis showed consistent differences in song structure between open and closed habitats. These differences were also found in an independent contrasts analysis, in which phylogenetic relationships between the species of the group were taken into account. In particular, the songs of species living in open habitats had wider bandwidths and higher maximum frequencies than those of species living in more closed habitats. In addition, the songs of open-habitat species had more notes, which were of shorter duration. These findings are compatible with predictions derived from the Acoustic Adaptation Hypothesis, according to which bird song structure is adapted to the habitat in which the signal is used.

DNA Barcode Libraries Provide Insight into Continental Patterns of Avian Diversification

Background The causes for the higher biodiversity in the Neotropics as compared to the Nearctic and the factors promoting species diversification in each region have been much debated. The refuge hypothesis posits that high tropical diversity reflects high speciation rates during the Pleistocene, but this conclusion has been challenged. The present study investigates this matter by examining continental patterns of avian diversification through the analysis of large-scale DNA barcode libraries. Methodology and Principal Findings Standardized COI datasets from the avifaunas of Argentina, the Nearctic, and the Palearctic were analyzed. Average genetic distances between closest congeners and sister species were higher in Argentina than in North America reflecting a much higher percentage of recently diverged species in the latter region. In the Palearctic genetic distances between closely related species appeared to be more similar to those of the southern Neotropics. Average intraspecific variation was similar in Argentina and North America, while the Palearctic fauna had a higher value due to a higher percentage of variable species. Geographic patterning of intraspecific structure was more complex in the southern Neotropics than in the Nearctic, while the Palearctic showed an intermediate level of complexity. Conclusions and Significance DNA barcodes can reveal continental patterns of diversification. Our analysis suggests that avian species are older in Argentina than in the Nearctic, supporting the idea that the greater diversity of the Neotropical avifauna is not caused by higher recent speciation rates. Species in the Palearctic also appear to be older than those in the Nearctic. These results, combined with the patterns of geographic structuring found in each region, suggest a major impact of Pleistocene glaciations in the Nearctic, a lesser effect in the Palearctic and a mild effect in the southern Neotropics.

Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird, Zonotrichia capensis

BackgroundThe Neotropics are exceptionally diverse, containing roughly one third of all extant bird species on Earth. This remarkable species richness is thought to be a consequence of processes associated with both Andean orogenesis throughout the Tertiary, and climatic fluctuations during the Quaternary. Phylogeographic studies allow insights into how such events might have influenced evolutionary trajectories of species and ultimately contribute to a better understanding of speciation. Studies on continentally distributed species are of particular interest because different populations of such taxa may show genetic signatures of events that impacted the continent-wide biota. Here we evaluate the genealogical history of one of the world’s most broadly-distributed and polytypic passerines, the rufous-collared sparrow (Zonotrichia capensis).ResultsWe obtained control region DNA sequences from 92 Zonotrichia capensis individuals sampled across the species’ range (Central and South America). Six additional molecular markers, both nuclear and mitochondrial, were sequenced for a subset of individuals with divergent control region haplotypes. Median-joining network analysis, and Bayesian and maximum parsimony phylogenetic analyses all recovered three lineages: one spanning Middle America, the Dominican Republic, and north-western South America; one encompassing the Dominican Republic, Roraima (Venezuela) and La Paz (Bolivia) south to Tierra del Fuego, Argentina; and a third, including eastern Argentina and Brazil. Phylogenetic analyses suggest that the Middle American/north-western South American clade is sister to the remaining two. Bayesian and maximum likelihood coalescent simulations used to study lineage demographic history, diversification times, migration rates and population expansion together suggested that diversification of the three lineages occurred rapidly during the Pleistocene, with negligible gene flow, leaving genetic signatures of population expansions.ConclusionsThe Pleistocene history of the rufous-collared sparrow involved extensive range expansion from a probable Central American origin. Its remarkable morphological and behavioral diversity probably represents recent responses to local conditions overlying deeper patterns of lineage diversity, which are themselves produced by isolation and the history of colonization of South America.

A molecular phylogeny of the Sierra-Finches (Phrygilus, Passeriformes): extreme polyphyly in a group of Andean specialists.

The unparalleled avian diversity of the Neotropics has long been argued to be in large part the evolutionary consequence of the incredible habitat diversity and rugged topography of the Andes mountains. Various scenarios have been proposed to explain how the Andean context could have generated lineage diversification (e.g. vicariant speciation or parapatric speciation across vertical ecological gradients), yet further study on Andean taxa is needed to reveal the relative importance of the different processes. Here we use mitochondrial and nuclear DNA sequences to derive the first phylogenetic hypothesis for Phrygilus (Sierra-Finches), one of the most species-rich genera of mainly Andean passerines. We find strong evidence that the genus is polyphyletic, comprising four distantly related clades with at least nine other genera interspersed between them (Acanthidops, Catamenia, Diglossa, Haplospiza, Idiopsar, Melanodera, Rowettia, Sicalis and Xenodacnis). These four Phrygilus clades coincide with groups previously established mainly on the basis of plumage characters, suggesting single evolutionary origins for each of these. We consider the history of diversification of each clade, analyzing the timing of splitting events, ancestral reconstruction of altitudinal ranges and current geographical distributions. Phrygilus species origins date mainly to the Pleistocene, with representatives diversifying within, out of, and into the Andes. Finally, we explored whether Phrygilus species, especially those with broad altitudinal and latitudinal Andean distributions, showed phylogeographic structure. Our best-sampled taxon (Phrygilus fruticeti) exhibited no clear pattern; however, we found deep genetic splits within other surveyed species, with Phrygilus unicolor being the most extreme case and deserving of further research.

CRYPTIC DICHROMATISM AND SEASONAL COLOR VARIATION IN THE DIADEMED TANAGER

Abstract We studied the patterns of sexual dichromatism and seasonal variation in plumage color in the Diademed Tanager (Stephanophorus diadematus), a species previously considered devoid of variation in adult plumage. The general coloration of this species is dark blue-violet, with a white-blue and red crown. Plumage reflectance of seven body regions from 33 study skins belonging to adults of both sexes was measured. Reflectance values were used in a principal components analysis (PCA) and hue, short-wave chroma, and UV chroma were also measured directly on the spectra. Both PCA factor scores and these latter variables were subjected to two-way ANCOVAs with sex and season as main factors and the year of capture as a covariate. We found that crowns of males were significantly brighter than those of females. In addition, the nape, chest, and belly showed significant differences in spectral shape, with relatively greater short-wave reflectance and less long-wave reflectance in males than in females. Although sexes were alike in hue, they differed in chroma in almost all body regions. Brightness also differed between seasons, and contrary to our expectation nonbreeding birds were brighter than breeding ones. This result may be a consequence of the particular molt program of tanagers that includes only a complete post-reproductive molt. Despite finding seasonal differences in spectral shape in various body regions, no significant changes in hue, short-wave chroma, or UV chroma were evident. To our knowledge, this is the first report of variation in adult plumage color for the Diademed Tanager, and we suggest that dichromatism in tanagers may be even more pervasive than is currently recognized. Dicromatismo Críptico y Variación Estacional de Color en Stephanophorus diadematus Resumen. Estudiamos los patrones de dicromatismo sexual y variación estacional en la coloración del plumaje de Stephanophorus diadematus, una especie previamente considerada carente de variación en la coloración del plumaje adulto. La coloración general de esta especie es azul violáceo oscuro, con una corona blanca azulada y roja. Se midió la reflectancia de siete regiones corporales en 33 pieles de estudio pertenecientes a adultos de ambos sexos. Los valores de reflectancia se utilizaron en un análisis de componentes principales, y además se midieron el tono (hue), la intensidad del color de onda corta y la intensidad del color de UV directamente sobre los espectros. Tanto los factores del análisis de componentes principales como las variables mencionadas fueron sujetos a ANCOVAs de dos factores, considerando el sexo y la estación como factores principales, y el año de captura como covariable. Estos análisis mostraron que la corona de los machos es significativamente más brillante que la de las hembras. Además, la nuca, el pecho y el vientre mostraron diferencias significativas en la forma espectral, presentando los machos mayor reflectancia en la zona de onda corta y menor en la zona de onda larga que las hembras. Si bien el tono no difirió entre sexos, la intensidad del color difirió en la mayoría de las regiones corporales entre machos y hembras. El brillo también difirió entre temporadas y, contrariamente a nuestra expectativa, los individuos capturados en la temporada no reproductiva fueron más brillantes que aquellos capturados en la temporada reproductiva. Este resultado podría deberse al programa de muda particular presente en Thraupidae, que incluye una única muda post-reproductiva completa. Si bien encontramos diferencias entre estaciones en la forma espectral en varias regiones corporales, no se detectaron diferencias en el tono, la intensidad del color de onda corta ni la intensidad del color de UV. Este es, de acuerdo a nuestro conocimiento, el primer estudio que muestra variación en la coloración del plumaje adulto de S. diadematus. Sugerimos que el dicromatismo en Thraupidae podría ser más común de lo que actualmente se piensa.