Search bioRxiv⌕ Search

Biology subjects

Bowie, R. C. K.

Publications and source records attributed to Bowie, R. C. K..

12 recordsLinked to original sources

A new avian feeding mechanism: Nectar suction by sunbirds

Nectarivory has independently evolved many times among birds, yet little is known about the diversity of feeding mechanisms that enable specialized taxa to efficiently collect this energyrich resource. Multiple avian groups have converged on evolving elongated bills and tube-like tongues adapted for nectar extraction. Old World sunbirds (family Nectariniidae) stand out as having the greatest degree of convergence in bill and tongue morphology with the well-studied and highly-specialized New World hummingbirds (family Trochilidae) which fill their tongues via elastic filling. However, using museum specimens, high-speed video, and fluid modeling, we show that sunbirds use a previously undescribed and unique drinking mechanism not found in any other animal: intralingual suction through the inside of hollow tubular tongues, a remarkable feat for animals without lips or cheeks.

biophysics↗

Remarkably high repeat content in the genomes of sparrows: the importance of genome assembly completeness for transposable element discovery.

Transposable elements (TE) play critical roles in shaping genome evolution. However, the highly repetitive sequence content of TEs is a major source of assembly gaps. This makes it difficult to decipher the impact of these elements on the dynamics of genome evolution. The increased capacity of long-read sequencing technologies to span highly repetitive regions of the genome should provide novel insights into patterns of TE diversity. Here we report the generation of highly contiguous reference genomes using PacBio long read and Omni-C technologies for three species of sparrows in the family Passerellidae. To assess the influence of sequencing technology on TE annotation, we compared these assemblies to three chromosome-level sparrow assemblies recently generated by the Vertebrate Genomes Project and nine other sparrow species generated using a variety of short- and long-read technologies. All long-read based assemblies were longer in length (range: 1.12-1.41 Gb) than short-read assemblies (0.91-1.08 Gb). Assembly length was strongly correlated with the amount of repeat content, with longer genomes showing much higher levels of repeat content than typically reported for the avian order Passeriformes. Repeat content for the Bells sparrow (31.2% of genome) was the highest level reported to date for a songbird genome assembly and was more in line with woodpecker (order Piciformes) genomes. CR1 LINE elements retained from an expansion that occurred 25-30 million years ago were the most abundant TEs in the song sparrow genome. Although the other five sparrow species also exhibit evidence for a spike in CR1 LINE activity at 25-30 million years ago, LTR elements stemming from more recent expansions were the most abundant elements in these species. LTRs were uniquely abundant in the Bells sparrow genome deriving from two recent peaks of activity. Higher levels of repeat content (79.2-93.7%) were found on the W chromosome relative to the Z (20.7-26.5) or autosomes (16.1-30.9%). These patterns support a dynamic model of transposable element expansion and contraction underpinning the seemingly constrained and small sized genomes of birds. Our work highlights how the resolution of difficult-to-assemble regions of the genome with new sequencing technologies promises to transform our understanding of avian genome evolution.

genomics↗

Cranes soar on thermal updrafts behind cold fronts as they migrate across the sea

Thermal soaring conditions above the sea have long been assumed absent or too weak for terrestrial migrating birds, forcing large obligate soarers to take long detours and avoid sea crossing, and facultative soarers to cross exclusively by costly flapping flight. Thus, while atmospheric convection does develop at sea and is utilized by some seabirds, it has been largely ignored in avian migration research. Here we provide direct evidence for routine thermal soaring over open sea in the common crane, the heaviest facultative soarer known among terrestrial migrating birds. Using high-resolution biologging from 44 cranes tracked across their transcontinental migration over 4 years, we show that soaring characteristics and performance were no different over sea than over land in mid-latitudes. Sea-soaring occurred predominantly in autumn when large water-air temperature difference followed mid-latitude cyclones. Our findings challenge a fundamental paradigm in avian migration research and suggest that large soaring migrants avoid sea crossing not due to absence or weakness of thermals but due to their uncertainty and the costs of prolonged flapping. Marine cold air outbreaks, imperative to the global energy budget and climate system, may also be important for bird migration, calling for more multidisciplinary research across biological and atmospheric sciences.

ecology↗

Abundant Phenotypic Parallelism, Incomplete Lineage Sorting, and Introgression in Open-Habitat Chats

Insights into the processes underpinning convergent evolution advance our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin convergent evolution. Here, we were interested in understanding the processes involved in convergent evolution in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the pattern of abundant convergent evolution, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for a role of novel mutations in the evolution of these phenotypes. Together, our results suggest that convergent evolution in open-habitat chats involved diverse processes and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.

evolutionary biology↗

Spatial variation in population genomic responses to over a century of anthropogenic change within a tidal marsh songbird

Combating the current biodiversity crisis requires the accurate documentation of population responses to human-induced ecological change. To this end, museum collections preserve a record of population responses to anthropogenic change that can provide critical baseline data on patterns of genetic diversity, connectivity, and population structure. We leveraged spatially-replicated time series of specimens to document population genomic responses to the destruction of nearly 90% of coastal habitats occupied by the Savannah sparrow (Passerculus sandwichensis) in California. Spatial-temporal analyses of genetic diversity from 219 sparrows collected between 1889-2017 showed that the amount of habitat lost was not predictive of genetic diversity loss. Despite experiencing the greatest levels of habitat loss, we found that genetic diversity in the San Francisco Bay Area remained relatively high. Over the past century, immigration into the Bay Area from interior populations has also increased. This may have minimized genetic diversity declines, but likely led to the erosion of divergence at loci associated with tidal marsh adaptation. Tracing the genomic trajectories of multiple populations over time provided unique insights into how shifting patterns of gene flow through time in response to human-induced habitat loss may contribute to negative fitness consequences.

evolutionary biology↗

Plumage balances camouflage and thermoregulation in Horned Larks (Eremophila alpestris)

Animal coloration serves many biological functions and must therefore balance potentially competing selective pressures. For example, many animals have camouflage, in which coloration matches the visual background against which predators scan for prey. However, different colors reflect different amounts of solar radiation and may therefore have thermoregulatory implications as well. In this study, we examined geographic variation in dorsal patterning, color, and solar reflectance among Horned Larks (Eremophila alpestris) of the western United States. We found associations between dorsal plumage brightness, hue, and patterning relative to the soil conditions where specimens were collected. Specifically, brighter dorsal plumage corresponded to brighter soil, while redder, more saturated hues in dorsal plumage corresponded to redder soils. Furthermore, backs with more high-contrast patterning were more common among females and also associated with soil that had coarser soil fragments, suggesting that lark plumage has been selected to optimize background matching in different environments. We also found that larks exhibited higher solar reflectance in hotter and more arid environments, which lowers the water requirements for homeothermy. Taken together, these findings suggest that natural selection has balanced camouflage and thermoregulation in Horned Larks across a wide variety of soil types and abiotic conditions.

zoology↗

Genomic variation and population histories of spotted (Strix occidentalis) and barred (S. varia) owls

Spotted owls (SO, Strix occidentalis) are a keystone species inhabiting old-growth forests in Western North America. In recent decades, their populations have declined due to ongoing reductions in suitable habitat caused by logging, wildfires, and competition with the congeneric barred owl (BO, Strix varia). The northern spotted owl (subspecies S. o. caurina) has been listed as "threatened" under the Endangered Species Act since 1990. Here we present a comprehensive look at genetic variation to elucidate the population histories of SO and invading western BO. Specifically, we present an improved SO genome assembly, based on 10x and Bionano Genomics data, along with 51 high-coverage whole-genome sequences including 11 SO from two subspecies (caurina and occidentalis), 25 BO, 2 confirmed and 13 potential hybrids. We identified potential hybrids based on intermediate morphology and found them to be a mixture of pure BO, F1 hybrids, and F1 x BO backcrosses. Unlike previous studies reporting asymmetries in the species-specific genders of the parents of F1 hybrids, we did not observe any significant asymmetry. Within species, we found that Western BO genetic variation is not simply a subset of the genetic variation in Eastern BO, suggesting that the two groups have been genetically isolated for longer (thousands of years) than previously suspected (80-130 years). Similarly, we found evidence of substantial genetic differentiation between the two SO subspecies. Finally, our analyses suggest that Northern SO experienced a moderate population bottleneck around the end of the last glaciation, while BO population sizes have always been large.

evolutionary biology↗

Inferring punctuated evolution in the learned songs of African sunbirds

Signals used in animal communication, especially those that are learned, are thought to be prone to rapid and/or regular evolution. It has been hypothesized that the evolution of song learning in birds has resulted in elevated diversification rates, as learned song may be subject to especially rapid evolution, and song is involved in mate choice. However, we know little about the evolutionary modes of learned song divergence over timescales relevant to speciation. Here we provide evidence that aspects of the territorial songs of Eastern Afromontane sky island sunbirds Cinnyris evolve in a punctuated fashion, with periods of stasis, on the order of hundreds of thousands of years or more, broken up by strong evolutionary pulses. Stasis in learned songs is inconsistent with learned traits being subject to constant or frequent change, as would be expected if selection does not constrain song phenotypes, or if novel phenotypes are frequently advantageous. Learned song may instead follow a process resembling peak shifts on adaptive landscapes. While much research has focused on the potential for rapid evolution in bird song, our results suggest that selection can tightly constrain the evolution of learned songs over fairly long timescales. More broadly, these results demonstrate that some aspects of highly variable, plastic traits can exhibit punctuated evolution, with stasis over fairly long time periods.

evolutionary biology↗

A comparison of visual features used by humans and machines to classify wildlife

In our quest to develop more intelligent machines, knowledge of the visual features used by machines to classify objects shall be helpful. The current state of the art in training machines to classify wildlife species from camera-trap data is to employ convolutional neural networks (CNN) encoded within deep learning algorithms. Here we report on results obtained in training a CNN to classify 20 African wildlife species with an overall accuracy of 87.5% from a dataset containing 111,467 images. We then used a gradient-weighted class-activation-mapping (Grad-CAM) procedure to extract the most salient pixels in the final convolution layer. We show that these pixels highlight features in particular images that are in most, but not all, cases similar to those used to train humans to identify these species. Further, we used mutual information methods to identify the neurons in the final convolution layer that consistently respond most strongly across a set of images of one particular species, and we then interpret the features in the image where the strongest responses occur. We also used hierarchical clustering of feature vectors (i.e., the state of the final fully-connected layer in the CNN) associated with each image to produce a visual similarity dendrogram of identified species. Finally, we evaluated how images that were not part of the training set fell within our dendrogram when these images were one of the 20 species \"known\" to our CNN in contrast to where they fell when these images were \"unknown\" to our CNN.

ecology↗

Whole-genome analysis of introgression between the spotted owl and barred owl (Strix occidentalis and Strix varia, respectively; Aves: Strigidae) in western North America

As the barred owl (Strix varia; Aves: Strigiformes: Strigidae) expands throughout western North America, hybridization between barred and spotted owls (Strix varia and S. occidentalis, respectively), if abundant, may lead to genetic swamping of the endangered spotted owl. We analyzed low-coverage, whole-genome sequence data from fifty-one barred and spotted owls to investigate recent introgression between these two species. Although we obtained genomic confirmation that these species can and do hybridize and backcross, we found no evidence of widespread introgression. Plumage characteristics of western S. varia that suggested admixture with S. occidentalis appear unrelated to S. occidentalis ancestry and may instead reflect local selection.

genomics↗

Whole-genome sequences suggest long term declines of spotted owl (Strix occidentalis) (Aves: Strigiformes: Strigidae) populations in California

We analyzed whole-genome data of four spotted owls (Strix occidentalis) to provide a broad-scale assessment of the genome-wide nucleotide diversity across S. occidentalis populations in California. We assumed that each of the four samples was representative of its population and we estimated effective population sizes through time for each corresponding population. Our estimates provided evidence of long-term population declines in all California S. occidentalis populations. We found no evidence of genetic differentiation between northern spotted owl (S. o. caurina) populations in the counties of Marin and Humboldt in California. We estimated greater differentiation between populations at the northern and southern extremes of the range of the California spotted owl (S. o. occidentalis) than between populations of S. o. occidentalis and S. o. caurina in northern California. The San Diego County S. o. occidentalis population was substantially diverged from the other three S. occidentalis populations. These whole-genome data support a pattern of isolation-by-distance across spotted owl populations in California, rather than elevated differentiation between currently recognized subspecies.

genomics↗

Taxonomy, phylogeny and biogeography of African spurfowls (Galliformes, Phasianidae, Coturnicinae, Pternistis spp.)

During much of the 20th Century, partridge/quail-like, Afro-Asian phasianine birds referred to commonly as African spurfowls, francolins and/or partridges had a tortuous taxonomic history. Because of striking autapomorphic differences in plumage, vocalizations and ecology in some of these taxa, as many as nine genera and nearly 200 clinal and/or idiosyncratic subspecies, embedded within a polyphyletic Perdicinae, were recognized. In 1963, two clades, 28 francolin and spurfowl species (fisante in Afrikaans) and 13 Afro-Asiatic francolins and partridges (patryse in Afrikaans), were combined into a single genus (Francolinus) - the largest within the Galliformes - comprising about 100 subspecies. Furthermore, fisante and patryse were partitioned into several unnamed \"Groups\" and four \"Unplaced\" species. Here, we use morphological, behavioural and DNA evidence to produce: a comprehensive revision of the taxonomy and phylogeny of the fisante clade; a stable classification system for tis component taxa; and hypotheses vis-a-vis eco-biogeographical processes that promoted their speciation and cladogenesis. We shift Francolinus spp. sensu stricto (members of the Spotted Group) and the Unplaced Francolinus gularis from the fisante clade to the patryse [discussed in Mandiwana-Neudani et al., in review]. An Unplaced fisant, F. nahani, is linked with Ptilopachus petrosus (another African endemic partridge ) within the Odontophoridae (New World Quails ). We recognize 25 species of fisante (hereafter spurfowls), including seven with subspecies. They comprise 34 terminal taxa placed within a single genus, Pternistis, sister to Ammoperdix and Perdicula spp., Coturnix quails and Alectoris partridges , within the now monophyletic Coturnicinae. Only one of four putative Groups of spurfowls, the Bare-throated Group, is monophyletic. The other three Groups (Montane, Scaly and Vermiculated) are para- or polyphyletic. Several species pairs of spurfowls, most notably P. afer and cranchii, hybridize in para/sympatry. One Bare-throated spurfowl, P. rufopictus, may be the product of stabilized hybridization between P. afer and/or cranchii and P. leucoscepus.

evolutionary biology↗