UC Berkeley

Nectar-feeding birds have enchanted scientists for centuries due to the remarkable morphological similarities between geographically and phylogenetically distant lineages, extreme life histories, and adaptations to a sugary diet. Though many characters have been attributed to the success of this ecological niche, no singular adaptation is shared across all radiations. Nectarivores range greatly in terms of body size, bill size and shape, tongue morphology, ecology, feeding behavior, and diet composition. Here, I assess nectarivory in birds as a syndrome through the lenses of feeding morphology, genetics, and nutritional ecology. I sought to better understand the evolution of nectarivory by investigating three different aspects of nectar-feeding adaptations: (1) tongues for transporting nectar into the throat; (2) the evolution of genes underlying bill morphology; and (3) the ecology of ethanol in the diets of birds. In chapters 1 and 2, I explore the skeletal morphology of the feeding apparatus and the genetic underpinnings of bill size and shape in Sunbirds (Passeriformes: Nectariniidae). In Chapter 3, I measure the prevalence of ethanol, a by-product of the fermentation of the sugars in nectar, with a focus on birds that feed on nectar and fruit. Specifically, I compare the prevalence of dietary ethanol within several species of hummingbirds and between hummingbirds and other bird species that serve as exemplars of other diet categories.In Chapter 1, I describe the tongue apparatus in sunbirds and explore the patterns of size and shape variation in the morphology of the skeletal elements using several phylogenetic comparative methods. When compared to their non-nectarivorous relatives, sunbirds have evolved a highly modified tongue apparatus to feed on nectar, yet sunbird species vary in the degree to which they specialize on nectar. To better understand the evolution of sunbird tongues, I first described the sunbird tongue apparatus and the function of key components by reconstructing the skeletal elements and associated soft tissues in situ of an Olive Sunbird (Cyanomitra olivacea). The functional significance of sunbird tongue morphology in nectar-feeding was hypothesized by comparing it to previous studies of avian tongue anatomy and function. Then I investigate patterns in morphological diversity across sunbirds and the relationship between size and shape, phylogeny, and feeding ecology by reconstructing the tongue skeleton from 41 CT scans representing sunbirds (Nectariniidae), flowerpeckers (Dicaeidae), and their relatives (Irenidae, Chloropseidae, Modulatricidae, Promeropidae). Two-dimensional and three-dimensional morphometrics were used to quantify size of the individual skeletal elements and the shape of the basihyal-urohyal. Two-dimensional data were supplemented with previously published bill measurements and body masses in the AVONET dataset. The morphology of the Olive Sunbird tongue apparatus supports previous hypotheses that sunbirds feed on nectar by generating a negative-pressure space (hermetic suction) with the tongue body and upper palate. I also describe a structure on the paraglossalia unique to sunbirds that likely provides structural support to the tongue body. The morphometric results suggest a complex interplay between bill size, tongue size and shape, and diet (as a proxy for feeding behavior) that is partially driven by phylogenetic history. Diet predicts shape depending on how body mass is included as a co-variable. Lastly, I compare the tongue apparatus between other nectarivorous radiations - hummingbirds and Australian honeyeaters - and discuss the differences in form and function of nectar-feeding adaptations across birds. In Chapter 2, I explore whether known candidate genes for bill morphology are implicated in the evolution of sunbird bills. Selection is expected to have occurred at the ancestral branch of sunbirds after the split from flowerpeckers (Dicaeidae) which coincides with an increase in bill length. I surveyed genes previously implicated in studies of bill size and shape. I generated sequence data of 11 candidate genes and phylogenetically informative sites for 139 taxa using a target capture method, including sunbirds (Nectariniidae), flowerpeckers, and several outgroups. Using a multilocus phylogeny constructed from the same individuals, exonic regions of these genes were tested for positive selection at the site level and at the branch level. I found evidence of episodic positive selection at a total of 28 sites across the protein ALX1, BMP4, LPP, RNASEH2B, and SHH. Fourteen sites were detected in LPP alone, six of which occurred in one exon, and seven were detected in RNASEH2B. No statistically significant, elevated rates of evolution was detected for the ancestral branch of sunbirds, nor for any other clades with elongated beaks. Although positive selection was not detected where I hypothesized, the results do not preclude these genes potentially being implicated in phenotypic changes in other ways (e.g., changes in gene expression). Chapter 3 focuses on the nutritional ecology of feeding on nectar. Ethanol is a naturally occurring molecule produced via fermentation of sugar-rich foods by yeast. Birds that regularly consume fruit and nectar may accordingly be ingesting ethanol on a chronic basis, although this possibility has not been documented in the wild. However, ethanol catabolism is followed by production of secondary metabolites such as ethyl glucuronide (EtG), which can be measured to provide a retrospective view of dietary exposure. We hypothesized that avian species with diets rich in fermentable sugars consume non-trivial amounts of ethanol, and therefore accumulate detectable levels of EtG. Assays for the presence of EtG in avian feathers yielded positive results for 10 of 17 avian species; EtG was also present at substantial levels in the livers of two of five study species. We found that EtG was present in nectarivorous hummingbirds, but also in species in other trophic niches (3 granivores, 1 omnivore, 3 invertivores, and 1 vertivore). Dietary exposure to ethanol may thus be much more widespread than has previously been recognized, and diverse features of avian nutritional ecology (e.g., secondary consumption via ingestion of prey items) may contribute to its accumulation in tissues.