Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks

Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α‐diversity. To calculate the PSS index, we then compare observed partner phylogenetic α‐diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host–parasite, avian seed‐dispersal, lichenized fungi–cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much‐needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss.     

Correlations between anthocyanin chemistry and pollination ecology in the polemoniaceae

A study of the anthocyanins in a representative sample (34 species from 14 genera) of Polemoniaceae has shown that the pigment type in the flowers is broadly correlated with pollination ecology. Thus, hummingbird pollinated species such as Ipomopsis aggregata generally contain pelargonidin sometimes with cyanidin, while bee and beefly pollinated species (e.g. Gilia latiflora) contain mainly delphinidin. On the other hand, lepidopteran species such as Leptodactylon californicum have cyanidin or mixtures of cyanidin with delphinidin. The above three anthocyanidins occur usually as the 3-glucoside, 3,5-diglucoside, $\text{3-(p-}\text{coumarylglucoside}\text{)}$ and $\text{3-(p-}\text{coumarylglucoside}\text{)-5-}\text{glucoside}$, although other types are occasionally found. The distribution of glycosidic types and of acylation, unlike that of the anthocyanidins, is more closely correlated with systematic position than with pollinating vectors. In autogamous species where animal pollination is absent or unimportant, anthocyanin pigmentation in the flowers retains the complexity present in related animal-pollinated taxa. Anthocyanins were also identified in hummingbird pollinated plants from two related families and pelargonidin derivatives were detected. In Fouquieria splendens (Fouquieriaceae), the glycosidic pattern was different from that in Polemoniaceae in being 3-galactoside. In Penstemon (Scrophulariaceae) a study of flower anthocyanins was consistent with Straw's hypothesis that the wasp-pollinated P. spectabilis originated by hybridization between the hummingbird-pollinated P. centranthifolius and the bee-pollinated P. grinnellii.     

Marking ruby-throated hummingbirds with radio frequency identification tags

We assessed the feasibility of marking ruby-throated hummingbirds (Archilochus colubris) with radio frequency identification (RFID) tags. We trapped 27 hummingbirds at feeding stations on a 2.0-ha study site. We subcutaneously implanted each hummingbird with a 0.067-g RFID tag and released it at the capture site. We deployed RFID transceiver systems at 5 feeding stations and electronically monitored tagged hummingbird activity continuously on the study site through 3 summers. Post-release relocation rate exceeded expectations based on previous leg band recovery data, and bird activity data acquisition was consistent and reliable and required minimum labor. © 2011 The Wildlife Society.     

Pollination biology and breeding system of Zeyheria montana (Bignoniaceae)

The reproductive biology of Zeyheria montana was studied through field observations of flower visitors and floral events, controlled manual pollinations, and observations of pollen tube growth and ovule penetration by fluorescence microscopy. Analysis of secretory areas of the nectar chamber was made by flower dissections and histology of serial sections. The flower lasted 6–8 days, but pollen exposure and stigma receptivity occurred only up to the end of the first and second days, respectively. Pollination was effected by several species of hummingbirds, especially Colibri serrirostris. The flowers present a rudimentary, non-functional disc, and secretion of nectar is performed by corolla-borne glandular trichomes. Only hand cross-pollinated and natural-pollinated flowers set fruits. Artificially self-pollinated and non-pollinated flowers dried off after anthesis without presenting any swelling of the ovary. Almost all the ovules in selfed and crossed pistils were penetrated 96 h after pollination. However, a delay in ovule penetration in self-pollinated pistils was verified, which indicates the occurrence of late-acting self-incompatibility.We are grateful to Fundo de Apoio ao Ensino e à Pesquisa (UNICAMP) for financial support, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the fellowship granted to the first author (this work is part of a Ph.D. thesis presented to UNICAMP, Campinas, SP, Brazil).     

DNA from a 100-year-old holotype confirms the validity of a potentially extinct hummingbird species

We used mtDNA sequence data to confirm that the controversial 100-year-old holotype of the Bogotá sunangel (Heliangelus zusii) represents a valid species. We demonstrate that H. zusii is genetically well differentiated from taxa previously hypothesized to have given rise to the specimen via hybridization. Phylogenetic analyses place H. zusii as sister to a clade of mid- to high-elevation Andean species currently placed in the genera Taphrolesbia and Aglaiocercus. Heliangelus zusii, presumed extinct, has never been observed in nature by biologists. We infer that the species occupied a restricted distribution between the upper tropical and temperate zones of the northern Andes and that it was most probably driven to extinction by deforestation that accompanied human population growth during the nineteenth and early twentieth centuries. We demonstrate the feasibility of obtaining DNA from nearly microscopic tissue samples from old hummingbird specimens and suggest that these methods could be used to resolve the taxonomy of dozens of avian taxa known only from type specimens.     

Community-wide assessment of pollen limitation in hummingbird-pollinated plants of a tropical montane rain forest

Background and Aims

Although pollen limitation of reproduction (PL) has been widely studied, our understanding of its occurrence in tropical communities, especially for bird-pollinated plants, is underdeveloped. In addition, inclusion of both quantity and quality aspects in studies of PL are generally lacking. Within hummingbird-pollinated plants, a prediction was made for higher PL for the quality than quantity aspects and a minor effect of temporal variation because hummingbirds are constant and efficient pollen vectors but they may transfer low quality pollen.

Methods

Field hand and open pollination experiments were conducted on 21 species in a tropical montane rain forest over 2 years. The quantity (fruit set and seeds per fruit) and quality (seed weight and germination) aspects of reproduction were assessed as the response to open pollination relative to outcross hand pollination. The relationships between the effect size of quantity and quality aspects of reproduction and predictive plant features (self-incompatibility, autogamy, density and pollinator specialization level) were assessed with phylogenetic generalized linear models.

Key Results

Just over half of all the species expressed PL for one or more response variables. On average, the severity of PL was strong for one quality variable (seed germination; 0·83), but insignificant for another (seed weight; –0·03), and low to moderate for quantity variables (0·31 for seeds per fruit and 0·39 for fruit set). There was only a minor contribution of temporal variation to PL within the studied species. Common predictors of PL, i.e. phylogenetic relatedness, self-incompatibility, autogamy, plant density and pollinator specialization level, did not adequately explain variation in PL within this community.

Conclusions

Despite the measurable degree of PL within these hummingbird-pollinated plants, the causes of pollen quality and quantity insufficiency are not clear. Variables other than those tested may contribute to PL or causes of PL may vary among species and cannot adequately be accounted for when assessed from the within-community perspective.     

The role of geography and ecology in shaping the phylogeography of the speckled hummingbird (Adelomyia melanogenys) in Ecuador

The Andes of South America contain one of the richest avifaunas in the world, but little is known about how this diversity arises and is maintained. Variation in mitochondrial DNA and morphology within the speckled hummingbird (Adelomyia melanogenys) was used to elucidate the phylogeographic pattern along an Ecuadorian elevational gradient, from the coastal cordillera to the inland Andean montane region. We examined sequence, climatic/remote sensing and morphological data to understand the effects of topography and ecology on patterns of variation. Populations on either side of the Andes are genetically divergent and were separated during a period that corresponds to the final stages of Andean uplift during the Pliocene. Despite isolation, these two populations were found to be morphologically similar suggesting a strong effect of stabilizing selection across ecologically similar Andean cloud forests, as assessed using climatic and remote sensing data. In contrast, little genetic divergence was found between coastal and west-Andean individuals, suggesting recent interruption of gene flow between these localities. However, coastal populations were found to inhabit different habitats compared to Andean populations as shown by climatic and remote sensing variables. Furthermore, coastal individuals had significantly longer bills compared to their montane relatives, indicative of differential directional selection and the influence of habitat differences in shaping phenotypic variation. Results highlight the role of both isolation and ecology in diversification in Ecuadorian montane regions, while suggesting the two may not always act in concert to produce divergence in adaptive traits.     

Synergism,Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

Sensory receptor evolution can imply trade-offs between ligands, but the extent to which such trade-offs occur and the underlying processes shaping their evolution is not well understood. For example, hummingbirds have repurposed their ancestral savory receptor (T1R1–T1R3) to detect sugars, but the impact of this sensory shift on amino acid perception is unclear. Here, we use functional and behavioral approaches to show that the hummingbird T1R1–T1R3 acts as a bifunctional receptor responsive to both sugars and amino acids. Our comparative analyses reveal substantial functional diversity across the hummingbird radiation and suggest an evolutionary timeline for T1R1–T1R3 retuning. Finally, we identify a novel form of synergism between sugars and amino acids in vertebrate taste receptors. This work uncovers an unexplored axis of sensory diversity, suggesting new ways in which nectar chemistry and pollinator preferences can coevolve.