Jacob M. Musser

Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines

Ultraviolet (UV) light-transmitted signals play a major role in avian foraging and communication, subserving functional roles in feeding, mate choice, egg recognition, and nestling discrimination. Sequencing functionally relevant regions of the short wavelength sensitive type 1 (SWS1) opsin gene that is responsible for modulating the extent of SWS1 UV sensitivity in birds allows predictions to be made about the visual system’s UV sensitivity in species where direct physiological or behavioral measures would be impractical or unethical. Here, we present SWS1 segment sequence data from representative species of three avian lineages for which visually based cues for foraging and communication have been investigated to varying extents. We also present a preliminary phylogenetic analysis and ancestral character state reconstructions of key spectral tuning sites along the SWS1 opsin based on our sequence data. The results suggest ubiquitous ultraviolet SWS1 sensitivity (UVS) in both paleognaths, including extinct moa (Emeidae), and parrots, including the nocturnal and flightless kakapo (Strigops habroptilus), and in most, but not all, songbird (oscine) lineages, and confirmed violet sensitivity (VS) in two suboscine families. Passerine hosts of avian brood parasites were included both UVS and VS taxa, but sensitivity did not co-vary with egg rejection behaviors. The results should stimulate future research into the functional parallels between the roles of visual signals and the genetic basis of visual sensitivity in birds and other taxa.

Nuclear β‐catenin localization supports homology of feathers, avian scutate scales, and alligator scales in early development

Feathers are an evolutionary novelty found in all extant birds. Despite recent progress investigating feather development and a revolution in dinosaur paleontology, the relationship of feathers to other amniote skin appendages, particularly reptile scales, remains unclear. Disagreement arises primarily from the observation that feathers and avian scutate scales exhibit an anatomical placode—defined as an epidermal thickening—in early development, whereas alligator and other avian scales do not. To investigate the homology of feathers and archosaur scales we examined patterns of nuclear β‐catenin localization during early development of feathers and different bird and alligator scales. In birds, nuclear β‐catenin is first localized to the feather placode, and then exhibits a dynamic pattern of localization in both epidermis and dermis of the feather bud. We found that asymmetric avian scutate scales and alligator scales share similar patterns of nuclear β‐catenin localization with feathers. This supports the hypothesis that feathers, scutate scales, and alligator scales are homologous during early developmental stages, and are derived from early developmental stages of an asymmetric scale present in the archosaur ancestor. Furthermore, given that the earliest stage of β‐catenin localization in feathers and archosaur scales is also found in placodes of several mammalian skin appendages, including hair and mammary glands, we hypothesize that a common skin appendage placode originated in the common ancestor of all amniotes. We suggest a skin placode should not be defined by anatomical features, but as a local, organized molecular signaling center from which an epidermal appendage develops.

Whole-body single-cell sequencing reveals transcriptional domains in the annelid larval body.

Abstract Animal bodies comprise diverse arrays of cells. To characterize cellular identities across an entire body, we have compared the transcriptomes of single cells randomly picked from dissociated whole larvae of the marine annelid Platynereis dumerilii. We identify five transcriptionally distinct groups of differentiated cells, each expressing a unique set of transcription factors and effector genes that implement cellular phenotypes. Spatial mapping of cells into a cellular expression atlas, and wholemount in situ hybridization of group‐specific genes reveals spatially coherent transcriptional domains in the larval body, comprising, for example, apical sensory‐neurosecretory cells versus neural/epidermal surface cells. These domains represent new, basic subdivisions of the annelid body based entirely on differential gene expression, and are composed of multiple, transcriptionally similar cell types. They do not represent clonal domains, as revealed by developmental lineage analysis. We propose that the transcriptional domains that subdivide the annelid larval body represent families of related cell types that have arisen by evolutionary diversification. Their possible evolutionary conservation makes them a promising tool for evo‐devo research.

Pervasive Correlated Evolution in Gene Expression Shapes Cell and Tissue Type Transcriptomes

Abstract The evolution and diversification of cell types is a key means by which animal complexity evolves. Recently, hierarchical clustering and phylogenetic methods have been applied to RNA-seq data to infer cell type evolutionary history and homology. A major challenge for interpreting this data is that cell type transcriptomes may not evolve independently due to correlated changes in gene expression. This nonindependence can arise for several reasons, such as common regulatory sequences for genes expressed in multiple tissues, that is, pleiotropic effects of mutations. We develop a model to estimate the level of correlated transcriptome evolution (LCE) and apply it to different data sets. The results reveal pervasive correlated transcriptome evolution among different cell and tissue types. In general, tissues related by morphology or developmental lineage exhibit higher LCE than more distantly related tissues. Analyzing new data collected from bird skin appendages suggests that LCE decreases with the phylogenetic age of tissues compared, with recently evolved tissues exhibiting the highest LCE. Furthermore, we show correlated evolution can alter patterns of hierarchical clustering, causing different tissue types from the same species to cluster together. To identify genes that most strongly contribute to the correlated evolution signal, we performed a gene-wise estimation of LCE on a data set with ten species. Removing genes with high LCE allows for accurate reconstruction of evolutionary relationships among tissue types. Our study provides a statistical method to measure and account for correlated gene expression evolution when interpreting comparative transcriptome data.

Loss and gain of cone types in vertebrate ciliary photoreceptor evolution

Ciliary photoreceptors are a diverse cell type family that comprises the rods and cones of the retina and other related cell types such as pineal photoreceptors. Ciliary photoreceptor evolution has been dynamic during vertebrate evolution with numerous gains and losses of opsin and phototransduction genes, and changes in their expression. For example, early mammals lost all but two cone opsins, indicating loss of cone receptor types in response to nocturnal lifestyle. Our review focuses on the comparison of specifying transcription factors and cell type-specific transcriptome data in vertebrate retinae to build and test hypotheses on ciliary photoreceptor evolution. Regarding cones, recent data reveal that a combination of factors specific for long-wavelength sensitive opsin (Lws)- cones in non-mammalian vertebrates (Thrb and Rxrg) is found across all differentiating cone photoreceptors in mice. This suggests that mammalian ancestors lost all but one ancestral cone type, the Lws-cone. We test this hypothesis by a correlation analysis of cone transcriptomes in mouse and chick, and find that, indeed, transcriptomes of all mouse cones are most highly correlated to avian Lws-cones. These findings underscore the importance of specifying transcription factors in tracking cell type evolution, and shed new light on the mechanisms of cell type loss and gain in retina evolution.

Pervasive concerted evolution in gene expression shapes cell type transcriptomes

Transcriptomic data yields valuable insights into cell type, tissue, and organ evolution. However, interpreting this data requires understanding how transcriptomes evolve. A particularly difficult problem is that cell type transcriptomes may not evolve independently. Here we present a statistical model to estimate the level of concerted transcriptome evolution and apply it to published and new data. The results indicate that tissues undergo pervasive concerted evolution in gene expression. Tissues related by morphology or developmental lineage exhibit higher levels of concerted evolution. Concerted evolution also causes tissues from the same species to be more similar in gene expression to each other than to homologous tissues in another species. This result may explain why some tissue transcriptomes cluster by species rather than homology. Our study illustrates the importance of accounting for concerted evolution when interpreting comparative transcriptome data, and should serve as a foundation for future investigations of cell type evolution.

Interspecific Competition in Grallaria Antpittas: Observations at a Feeder

Abstract We describe an aggressive interaction between the extremely rare Jocotoco Antpitta (Grallaria ridgelyi) and a close relative, the Chestnut-naped Antpitta (Grallaria nuchalis). Since first discovered in 1997, ecological information about the Jocotoco Antpitta has begun to accrue; however, much remains to be learned about this rare species in its limited native range. The observations described here advance our knowledge of the behavioral ecology of this elusive species and contribute more broadly to our knowledge of interspecific competition in antpittas in general. We show that in avian systems in which playback experiments fail to detect competition, competition may still be prevalent, in this case manifesting in a nonvocal, physically aggressive interaction. We also raise new questions about the potential for temporal variation in interspecific competition in grallariids due to increased resource demands during nestling provisioning.

Subdivision of ancestral scale genetic program underlies origin of feathers and avian scutate scales

Birds and other reptiles possess a diversity of feather and scale-like skin appendages. Feathers are commonly assumed to have originated from ancestral scales in theropod dinosaurs. However, most birds also have scaled feet, indicating birds evolved the capacity to grow both ancestral and derived morphologies. This suggests a more complex evolutionary history than a simple linear transition between feathers and scales. We set out to investigate the evolution of feathers via the comparison of transcriptomes assembled from diverse skin appendages in chicken, emu, and alligator. Our data reveal that feathers and the overlapping ‘scutate’ scales of birds share more similar gene expression to each other, and to two types of alligator scales, than they do to the tuberculate ‘reticulate’ scales on bird footpads. Accordingly, we propose a history of skin appendage diversification, in which feathers and bird scutate scales arose from ancestral archosaur body scales, whereas reticulate scales arose earlier in tetrapod evolution. We also show that many “feather-specific genes” are also expressed in alligator scales. In-situ hybridization results in feather buds suggest that these genes represent ancestral scale genes that acquired novel roles in feather morphogenesis and were repressed in bird scales. Our findings suggest that the differential reuse, in feathers, and suppression, in bird scales, of genes ancestrally expressed in archosaur scales has been a key factor in the origin of feathers – and may represent an important mechanism for the origin of evolutionary novelties.