Andean Hummingbirds Research Articles

Mito-nuclear discordance in the phenotypically variable Andean hummingbirdsCoeligena bonaparteiandCoeligena helianthea(Trochilidae)

AbstractThe interplay among evolutionary mechanisms like gene flow and selection may result in discordant signals between mitochondrial DNA, nuclear markers and phenotypes. The Andean hummingbirds Coeligena bonapartei and Coeligena helianthea showed differentiation in the gene ND2 which is discordant with plumage coloration but consistent with geography. We analysed complete mitochondrial genomes of individuals from Coeligena bonapartei bonapartei, Coeligena bonapartei consita, Coeligena helianthea helianthea, and Coeligena helianthea tamai to inform their evolutionary history. We found genetic structure despite low genetic differentiation among these populations. Phylogenetic and network analyses based on mitogenomes showed a northern vs. southern differentiation pattern which is discordant with the relationships based on nuclear markers and the coloration phenotypes (serving as a basis for taxonomy). Mitogenomes of the two nominate subspecies are indistinguishable, suggesting incomplete lineage sorting or introgression, while those of C. b. consita and C. h. tamai are more similar to each other than they are to their respective nominate subspecies. Our results indicate that various evolutionary mechanisms drove the divergence in phenotypes, and nuclear and mitochondrial genomes of Coeligena hummingbirds, playing out over a complex biogeographic scenario likely involving periods of isolation and secondary contact. We outline hypotheses to be tested with future analyses of genome-wide variation.

Ecological drivers and consequences of torpor in Andean hummingbirds.

Daily torpor allows endotherms to save energy during energetically stressful (e.g. cold) conditions. Although studies on avian torpor have mostly been conducted under laboratory conditions, information on the usage of torpor in the wild is limited to few, predominantly temperate-zone species. We studied torpor under seminatural conditions from 249 individuals from 29 hummingbird species across a 1920 m elevational gradient in the western Andes of Colombia using cloacal thermistors. Small birds were more likely to use torpor than large birds, but only at low ambient temperatures, where torpor was prolonged. We also found effects of proxy variables for body condition and energy expenditure on the use of torpor, its characteristics, and impacts. Our results suggest that context-dependency and phylogenetic variation in the probability of deploying torpor can help understand clade-wide patterns of elevational distribution in Andean hummingbirds.

Hummingbird community structure and nectar resources modulate the response of interspecific competition to forest conversion

On-going land-use change has profound impacts on biodiversity by filtering species that cannot survive in disturbed landscapes and potentially altering biotic interactions. In particular, how land-use change reshapes biotic interactions remains an open question. Here, we used selectivity experiments with nectar feeders in natural and converted forests to test the direct and indirect effects of land-use change on resource competition in Andean hummingbirds along an elevational gradient. Selectivity was defined as the time hummingbirds spent at high resource feeders when feeders with both low and high resource values were offered in the presence of other hummingbird species. Selectivity approximates the outcome of interspecific competition (i.e., the resource intake across competing species); in the absence of competition, birds should exhibit higher selectivity. We evaluated the indirect effect of forest conversion on selectivity, as mediated by morphological dissimilarity and flower resource abundance, using structural equation models. We found that forest conversion influenced selectivity at low and mid-elevations, but the influence of morphological dissimilarity and resource availability on selectivity varied between these elevations. At mid-elevation, selectivity was more influenced by the presence of morphologically similar competitors than by resource abundance while at low-elevation resource abundance was a more important predictor of selectivity. Our results suggest that selectivity is influenced by forest conversion, but that the drivers of these changes vary across elevation, highlighting the importance of considering context-dependent variation in the composition of resources and competitors when studying competition.

Biodiversity cradles and museums segregating within hotspots of endemism.

The immense concentrations of vertebrate species in tropical mountains remain a prominent but unexplained pattern in biogeography. A long-standing hypothesis suggests that montane biodiversity hotspots result from endemic species aggregating within ecologically stable localities. Here, the persistence of ancient lineages coincides with frequent speciation events, making such areas both 'cradles' (where new species arise) and 'museums' (where old species survive). Although this hypothesis refers to processes operating at the scale of valleys, it remains supported primarily by patterns generated from coarse-scale distribution data. Using high-resolution occurrence and phylogenetic data on Andean hummingbirds, we find that old and young endemic species are not spatially aggregated. The young endemic species tend to have non-overlapping distributions scattered along the Andean treeline, a long and narrow habitat where populations easily become fragmented. By contrast, the old endemic species have more aggregated distributions, but mainly within pockets of cloud forests at lower elevations than the young endemic species. These findings contradict the premise that biogeographical cradles and museums should overlap in valley systems where pockets of stable climate persist through periods of climate change. Instead, Andean biodiversity hotspots may derive from large-scale fluctuating climate complexity in conjunction with local-scale variability in available area and habitat connectivity.

Pervasive Genomic Signatures of Local Adaptation to Altitude Across Highland Specialist Andean Hummingbird Populations.

Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them "taller" biogeographic barriers.

Recent diversification in the high Andes: unveiling the evolutionary history of the Ecuadorian hillstar,Oreotrochilus chimborazo(Apodiformes: Trochilidae)

AbstractStudying the genetic signatures of evolutionary diversification in young lineages is among the most promising approaches for unveiling the processes behind speciation. Here, we focus on Oreotrochilus chimborazo, a high Andean species of hummingbird that might have experienced rapid diversification in the recent past. To understand the evolution of this species, we generated a dataset of ten microsatellite markers and complementary data on morphometrics, plumage variation and ecological niches. We applied a series of population and coalescent-based analyses to understand the population structure and differentiation within the species, in addition to the signatures of current and historical gene flow, the location of potential contact zones and the relationships among lineages. We found that O. chimborazo comprises three genetic groups: one corresponding to subspecies O. c. chimborazo, from Chimborazo volcano and surroundings, and two corresponding to the northern and southern ranges of subspecies O. c. jamesonii, found from the extreme south of Colombia to southern Ecuador. We inferred modest levels of both contemporary and historical gene flow and proposed the location of a contact zone between lineages. Also, our coalescent-based analyses supported a rapid split among these three lineages during the mid-to-late Holocene. We discuss our results in the light of past and present potential distributions of the species, in addition to evolutionary trends seen in other Andean hummingbirds.

Transmission of high-frequency vocalizations from hummingbirds living in diverse habitats

Abstract Some species of Andean hummingbirds produce high-frequency vocalizations which exceed the vocal range of most birds. They also challenge our understanding of the role of habitat structure in the evolution of vocal signals because these hummingbirds live in strikingly different habitats, ranging from cloud forest to high-altitude grasslands. Although these vocalizations are produced at high frequencies, they exhibit considerable variation in frequency content and temporal structure. The calls of the hummingbirds from the cloud forest are simpler and have a narrow frequency range compared to the complex song of the grasslands hummingbird. We hypothesized that each of the three high-frequency vocalizations is adapted for transmission in their habitat. We characterized the transmission of high-frequency vocal signals in the cloud forest and in the grasslands. All vocalizations attenuated and degraded substantially at short distances, suggesting that they are adapted for short-range communication. The simple vocalizations of the cloud-forest species transmitted better in both environments compared to the complex song of the grasslands hummingbird, probably due to relaxed constraints for high-frequency sounds in open habitats.

Extreme and variable torpor among high-elevation Andean hummingbird species.

Torpor is thought to be particularly important for small endotherms occupying cold environments and with limited fat reserves to fuel metabolism, yet among birds deep torpor is both rare and variable in extent. We investigated torpor in hummingbirds at approximately 3800 m.a.s.l. in the tropical Andes by monitoring body temperature (Tb) in 26 individuals of six species held captive overnight and experiencing natural air temperature (Ta) patterns. All species used pronounced torpor, with one Metallura phoebe reaching a minimum Tb of 3.26°C, the lowest yet reported for any bird or non-hibernating mammal. The extent and duration of torpor varied among species, with overnight body mass (Mb) loss negatively correlated with both minimum Tb and bout duration. We found a significant phylogenetic signal for minimum Tb and overnight Mb loss, consistent with evolutionarily conserved thermoregulatory traits. Our findings suggest deep torpor is routine for high Andean hummingbirds, but evolved species differences affect its depth.

Niches and radiations: a case study on the Andean sapphire‐vented puffleg Eriocnemis luciani and coppery‐naped puffleg E. sapphiropygia (Aves, Trochilidae)

The interaction between ecology and evolution, particularly with regard to speciation processes, remains a main topic of scientific research. Andean hummingbirds have undergone a remarkable radiation, with many species exhibiting patchy distributions and, in some cases, taxonomic controversy. An example is the sapphire‐vented puffleg Eriocnemis luciani; ssp. baptistae, luciani and meridae, which some authors merge with the coppery‐naped puffleg E. sapphiropygia; ssp. catharina and sapphiropygia. Each group is distributed either north or south from the Huancabamba Depression, the major biogeographical barrier within the tropical Andes. We investigated whether these subspecies share some niche characteristics despite their geographical separation and determined their meaning in the context of the speciation process of trochilids in the tropical Andes. For each subspecies, we performed geographical predictions and paired tests of niche conservatism in environmental space. Geographical predictions included separate regions for subspecies catharina and sapphiropygia, while the predicted regions for subspecies luciani and baptistae greatly overlapped. The E. l. luciani model predicted a single pixel near to the potential area of E. l. meridae, known only from a unique, old record. Subspecies luciani and baptistae exhibited the greatest niche overlap among the pairs of taxa for most variables. However, our results clearly indicated niche divergence for the four members of the E. luciani–sapphiropygia complex, independent of the similarities or slight dissimilarities in their respective backgrounds, indicating that other forces in addition to variation in environmental parameters, such as natural selection or genetic drift, are driving the radiation of these hummingbirds. This finding coincides with the unusually high speciation rates reported for Andean hummingbirds. Thus, the currently accepted taxonomy within the E. luciani–sapphiropygia complex may be even more convoluted than indicated by previous studies. Hence, the results of our study are a wakeup call to include the exploration of lineage diversification in biodiversity‐related efforts.

Shallow genetic divergence and distinct phenotypic differences between two Andean hummingbirds: Speciation with gene flow?

AbstractEcological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

Highlight: Andean Hummingbirds Reveal Distinct Evolutionary Pathways to High-Altitude Adaptation.

Highlight: Andean Hummingbirds Reveal Distinct Evolutionary Pathways to High-Altitude Adaptation.

Combining multiple sources of data to uncover the natural history of an endemic Andean hummingbird, the Peruvian Piedtail ( Phlogophilus harterti )

Combining multiple sources of data to uncover the natural history of an endemic Andean hummingbird, the Peruvian Piedtail ( <i>Phlogophilus harterti</i> )

Land use change has stronger effects on functional diversity than taxonomic diversity in tropical Andean hummingbirds.

Land use change modifies the environment at multiple spatial scales, and is a main driver of species declines and deterioration of ecosystem services. However, most of the research on the effects of land use change has focused on taxonomic diversity, while functional diversity, an important predictor of ecosystem services, is often neglected. We explored how local and landscape scale characteristics influence functional and taxonomic diversity of hummingbirds in the Andes Mountains in southern Ecuador. Data was collected in six landscapes along a land use gradient, from an almost intact landscape to one dominated by cattle pastures. We used point counts to sample hummingbirds from 2011 to 2012 to assessed how local factors (i.e., vegetation structure, flowering plants richness, nectar availability) and landscape factors (i.e., landscape heterogeneity, native vegetation cover) influenced taxonomic and functional diversity. Then, we analyzed environment – trait relationships (RLQ test) to explore how different hummingbird functional traits influenced species responses to these factors. Taxonomic and functional diversity of hummingbirds were positively associated with landscape heterogeneity but only functional diversity was positively related to native vegetation coverage. We found a weak response of taxonomic and functional diversity to land use change at the local scale. Environment‐trait associations showed that body mass of hummingbirds likely influenced species sensitivity to land use change. In conclusion, landscape heterogeneity created by land use change can positively influence hummingbird taxonomic and functional diversity; however, a reduction of native vegetation cover could decrease functional diversity. Given that functional diversity can mediate ecosystem services, the conservation of native vegetation cover could play a key role in the maintenance of hummingbird pollination services in the tropical Andes. Moreover, there are particular functional traits, such as body mass, that increase a species sensitivity to land use change.

On comparing traits and abundance for predicting species interactions with imperfect detection

To determine the causes, frequency and stability of biotic interactions, ecologists often use field observations to generate networks of interacting species. The challenge is in determining whether unobserved interactions were undetected due to sampling, or whether they truly do not occur. This uncertainty makes it difficult to predict interactions based on ecological mechanisms. By using hierarchical Bayesian N-mixture models adapted from wildlife ecology, we differentiated the probability of detecting a species from the intensity of species interactions. We began with a brief simulation to illustrate the consequences of ignoring detectability when building species networks. We then applied our model to an empirical dataset on Andean hummingbirds to compare trait-matching and plant abundance in explaining flower visitation patterns. The daily probability of detecting a hummingbird interaction ranged from 14% to 70% among species, underlining the importance of multiple days of sampling when estimating species interactions. The trait-matching model best fit hummingbird visitation rates among plants and pollinators. The plant abundance model was inconsistent across hummingbird species and did not support neutral interactions based on increasing plant abundance. We recommend that network studies account for interaction detectability by separately modeling observation and process mechanisms, focusing on species-level discrepancy in assessing model adequacy, and estimating uncertainty when computing network statistics.

Isolation and Characterisation of 11 Microsatellite Loci in the Ecuadorian Hillstar Oreotrochilus chimborazo

The Ecuadorian Hillstar Oreotrochilus chimborazo is a high Andean hummingbird that inhabits paramo ecosystems from extreme southern Colombia to southern Ecuador. The species is currently divided into three subspecies that differ in morphology and geographic distribution but no molecular differences have been found between them using mitochondrial markers. The aim of this study was to isolate and test microsatellite loci to further explore possible genetic variability between and within these subspecies. Screening an enriched genomic library of O. chimborazo we obtained eleven polymorphic microsatellite loci. These markers will be used to further elucidate evolutionary patterns in the species.

First nesting account and breeding biology of “Gould's Inca” (Coeligena torquata omissa) in Manu National Park, Peru

ABSTRACT We present the first detailed nesting biology information for the highland Andean hummingbird Gould's Inca (Coeligena torquata omissa) at 2,200–3,000 m in Manu National Park, SE Peru. We found nine mossy cup-shaped nests lined with red fern scales containing nestlings or 1–2 synchronously hatching eggs. We obtained 17 days of internal nest temperatures from one nest, which exhibited wide circadian variation (range = 14.9–36.2 °C). We show that C. t. omissa meets the challenges of life and incubation at high altitudes by undertaking numerous (20.3 ± 0.4 trips/morning, range = 14–27) and short morning off-bouts (5.2 ± 0.2 min, range = 1–24 min). In the morning, the focal bird warmed the nest 1.7 times faster than in the afternoon where incubation bouts are long (17.8 ± 0.6 min, range = 4–56) and less frequent (10.2 ± 0.3 trips/afternoon). Incubation off-bout frequency and durations were not influenced by external temperature, suggesting strong nest insulation. On-bout durations increased with exter...

Evaluating broad scale patterns among related species using resource experiments in tropical hummingbirds.

A challenge in community ecology is connecting biogeographic patterns with local scale observations. In Neotropical hummingbirds, closely related species often co-occur less frequently than expected (overdispersion) when compared to a regional species pool. While this pattern has been attributed to interspecific competition, it is important to connect these findings with local scale mechanisms of coexistence. We measured the importance of the presence of competitors and the availability of resources on selectivity at experimental feeders for Andean hummingbirds along a wide elevation gradient. Selectivity was measured as the time a bird fed at a feeder with a high sucrose concentration when presented with feeders of both low and high sucrose concentrations. Resource selection was measured using time-lapse cameras to identity which floral resources were used by each hummingbird species. We found that the increased abundance of preferred resources surrounding the feeder best explained increased species selectivity, and that related hummingbirds with similar morphology chose similar floral resources. We did not find strong support for direct agonism based on differences in body size or phylogenetic relatedness in predicting selectivity. These results suggest closely related hummingbird species have overlapping resource niches, and that the intensity of interspecific competition is related to the abundance of those preferred resources. If these competitive interactions have negative demographic effects, our results could help explain the pattern of phylogenetic overdispersion observed at regional scales.

Repeated elevational transitions in hemoglobin function during the evolution of Andean hummingbirds

Animals that sustain high levels of aerobic activity under hypoxic conditions (e.g., birds that fly at high altitude) face the physiological challenge of jointly optimizing blood-O2 affinity for O2 loading in the pulmonary circulation and O2 unloading in the systemic circulation. At high altitude, this challenge is especially acute for small endotherms like hummingbirds that have exceedingly high mass-specific metabolic rates. Here we report an experimental analysis of hemoglobin (Hb) function in South American hummingbirds that revealed a positive correlation between Hb-O2 affinity and native elevation. Protein engineering experiments and ancestral-state reconstructions revealed that this correlation is attributable to derived increases in Hb-O2 affinity in highland lineages, as well as derived reductions in Hb-O2 affinity in lowland lineages. Site-directed mutagenesis experiments demonstrated that repeated evolutionary transitions in biochemical phenotype are mainly attributable to repeated amino acid replacements at two epistatically interacting sites that alter the allosteric regulation of Hb-O2 affinity. These results demonstrate that repeated changes in biochemical phenotype involve parallelism at the molecular level, and that mutations with indirect, second-order effects on Hb allostery play key roles in biochemical adaptation.

Phoretic mites identified on andean hummingbirds (Trochilidae) of Caldas, Colombia

Within the bird-plant-mite system, the relationship between hummingbirds, flowers, and mites remains poorly understood. In this study, we evaluated the degree of association between nasal mites and eight species of Andean hummingbirds in Colombia (Amazilia saucerrottei, A. tzacatl, Chalybura buffonii, Chlorostilbon mellisugus, Florisuga mellivora, Glaucis hirsutus, Phaethornis guy and P. striigularis). Over a five-month period (trapping effort 360 hours/month), a total of 178 birds were captured, from which 81 mite specimens were collected and identified as belonging to three genera (Proctolaelaps, Rhinoseius and Tropicoseius) spanning eleven species. This is the first report of its kind from Colombia on the identification of the mite species P. rabulatus, R. luteyni, R. rafinskii, T. berryi, T. colwelli, T. erro and T. uniformis and the first record of P. guy as phoretic host for Proctolaelaps rabulatus. Morphological characteristics (length of the dorsal plate, width of the dorsal plate and setae z5 length) alone failed to distinguish between mite species. The ecologic impact of this relationship on flowers with respect to nectar and pollen availability and the effect of mites on pollination by hummingbirds needs to be determined.

Evolutionary patterns of diversification in the Andean hummingbird genus Adelomyia

The patterns of genetic diversity and morphological variation are of central importance in understanding the evolutionary process that drive diversification. We use molecular, morphological, and ecological data to explore the influence of geography and ecology in promoting speciation in the widespread Andean hummingbird genus Adelomyia. Six monophyletic clades were recovered which show distributional limits at well-defined geographic barriers. Percentage sequence divergence ranged between 5.8% and 8.2% between phylogroups separated by large (>4000 km) and small (<50 km) distances respectively, suggesting that geographic isolation may be influential at very different scales. We show that morphological traits in independent phylogroups are more related to environmental heterogeneity than to geographic barriers. We provide a molecular reconstruction of relationships within Adelomyia and recommend its use in future comparative studies of historical biogeography and diversification in the Andes.