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Toomey, M. B.

Publications and source records attributed to Toomey, M. B..

7 recordsLinked to original sources

Plumage diversity without differential expression of pigmentation genes in a rapid avian radiation

Uncovering the molecular basis of reproductive traits is key to understanding species divergence. Capuchino Seedeaters ( Sporophila ), a radiation of genetically similar birds differing mainly in male reproductive plumage color, can be leveraged to study how such traits evolve. Outlier scans identified candidate pigmentation variants primarily in noncoding sequence, implying regulatory changes. However, RNA-seq of growing feather follicles generally did not show differential expression of pigmentation genes among different colors, with only ASIP downregulated in crown feathers. Gene expression patterns instead varied by body region. The largest difference between dimorphic sexes was the upregulation of the carotenoid-degrading gene BCO2 in males, accompanied by lower carotenoid content in male feathers. An improved genome annotation assigned 9.5% of candidate variants into coding and untranslated sequence. This suggests species-diagnostic variants lie within transcribed sequence and could act post-transcriptionally, rather than through transcript abundance, leading to a revised hypothesis for plumage divergence in this radiation.

genomics↗

Multiple pathways to red carotenoid coloration: House finches(Haemorhous mexicanus) do not use CYP2J19 to produce red plumage

The carotenoid-based colors of birds are a celebrated example of biological diversity and an important system for the study of evolution. Recently, a two-step mechanism, with the enzymes cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L), was described for the biosynthesis of red ketocarotenoids from yellow dietary carotenoids in the retina and plumage of birds. A common assumption has been that all birds with ketocarotenoid-based plumage coloration used this CYP2J19/BDH1L mechanism to produce red feathers. We tested this assumption in house finches (Haemorhous mexicanus) by examining the catalytic function of the house finch homologs of these enzymes and tracking their expression in molting birds. We found that CYP2J19 and BDH1L did not catalyze the production of 3-hydroxy-echinenone (3-OH-echinenone), the primary red plumage pigment of house finches, when provided with common dietary carotenoid substrates. Moreover, gene expression analyses revealed little to no expression of CYP2J19 in liver tissue or growing feather follicles, the putative sites of pigment metabolism in molting house finches. Finally, although the hepatic mitochondria of house finches have high concentrations of 3-OH-echinenone, observations using fluorescent markers suggest that both CYP2J19 and BDH1L localize to the endomembrane system rather than the mitochondria. We propose that house finches and other birds that deposit 3-OH-echinenone as their primary red plumage pigment use an alternative enzymatic pathway to produce their characteristic red ketocarotenoid-based coloration.

evolutionary biology↗

Light environment and seasonal variation in the visual system of the red shiner (Cyprinella lutrensis)

The light environment underwater can vary dramatically over space and time, challenging the visual systems of aquatic organisms. To meet these challenges, many species shift their spectral sensitivities through changes in visual pigment chromophore and opsin expression. The red shiner (Cyprinella lutrensis) is a cyprinid minnow species that has rapidly expanded its range throughout North America and inhabits a wide range of aquatic habitats. We hypothesized that visual system plasticity has contributed to the red shiners success. We investigated plasticity in chromophore usage and opsin expression by collecting red shiners from three Oklahoma creeks that vary in turbidity throughout the year. We characterized the light environment by spectroradiometry, measured chromophore composition of the eyes with high performance liquid chromatography, characterized CYP27C1 enzyme function through heterologous expression, and examined ocular gene expression by RNA sequencing and de novo transcriptome assembly. We observed significantly higher proportions of the long- wavelength shifted A2 chromophore in the eyes of fish from the turbid site and in samples collected in winter, suggesting that there may be a temperature-dependent trade-off between chromophore-based spectral tuning and chromophore-related noise. Opsin expression varied between turbid and clear creeks, but did not align with light environment as expected, and the magnitude of these differences was limited compared to the differences in chromophore composition. We confirmed that red shiner CYP27C1 catalyzes the conversion of A1 to A2, but the ocular expression of CYP27C1 was not well correlated with A2 levels in the eye, suggesting conversion may be occurring outside of the eye.

physiology↗

Captivity affects mitochondrial aerobic respiration and carotenoid metabolism in the house finch (Haemorhous mexicanus)

In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation is an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity would affect both mitochondrial performance and the abundance of red carotenoids. We found no evidence that living in small versus large cages had significant effects on wild-caught house finches; however, birds in cages of any size circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios--a metric associated with mitochondrial efficiency--compared to free-living birds. Moreover, among captive individuals, the birds that circulated the most red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrates. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established. SUMMARY STATEMENTHolding wild-caught male house finches in cages exposed a relationship between red carotenoid production and mitochondrial respiratory efficiency.

evolutionary biology↗

Development and genetics of red coloration in the zebrafish relative Danio albolineatus

Animal pigment patterns play important roles in behavior and, in many species, red coloration serves as an honest signal of individual quality in mate choice. Among Danio fishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, we use pearl danio (D. albolineatus) to assess the developmental origin of erythrophores and their mechanisms of differentiation. We show that erythrophores in the fin of D. albolineatus share a common progenitor with xanthophores and maintain plasticity in cell fate even after differentiation. We further identify the predominant ketocarotenoids that confer red coloration to erythrophores and use reverse genetics to pinpoint genes required for the differentiation and maintenance of these cells. Our analyses are a first step towards defining the mechanisms underlying the development of erythrophore-mediated red coloration in Danio and reveal striking parallels with the mechanism of red coloration in birds.

developmental biology↗

Genetic Basis Of De Novo Appearance Of Carotenoid Ornamentation In Bare-Parts Of Canaries

AO_SCPCAPBSTRACTC_SCPCAPUnlike wild and domestic canaries (Serinus canaria), or any of the three dozen species of finches in genus Serinus, the domestic urucum breed of canaries exhibits bright red bills and legs. This novel bare-part coloration offers a unique opportunity to understand how leg and bill coloration evolve in birds. To identify the causative locus, we resequenced the genome of urucum canaries and performed a range of analyses to search for genotype-to-phenotype associations across the genome. We identified a nonsynonymous mutation in the gene BCO2 (beta-carotene oxygenase 2, also known as BCDO2), an enzyme involved in the cleavage and breakdown of full-length carotenoids into short apocarotenoids. Protein structural models and in vitro functional assays indicate that the urucum mutation abrogates the carotenoid cleavage activity of BCO2. Consistent with the predicted loss of carotenoid cleavage activity, urucum canaries had increased levels of full-length carotenoid pigments in bill tissue and a significant reduction in levels of carotenoid cleavage products (apocarotenoids) in retinal tissue compared to other breeds of canaries. We hypothesize that carotenoid-based bare-part coloration might be readily gained, modified, or lost through simple switches in the enzymatic activity or regulation of BCO2 and this gene may be an important mediator in the evolution of bare-part coloration among bird species.

evolutionary biology↗

Thyroid hormone regulates distinct paths to maturation in pigment cell lineages

Circulating endocrine factors are critical for orchestrating complex developmental processes during the generation of adult form. One such factor, thyroid hormone, regulates diverse cellular processes during post-embryonic development and can drive disparate morphological outcomes through mechanisms that remain essentially unknown. We sought to define how thyroid hormone elicits opposite responses in the abundance of two pigment cell classes during development of the zebrafish adult pigment pattern. By profiling individual transcriptomes from thousands of neural crest derived cells, including pigment cells, we reconstructed developmental trajectories and identified lineage-specific changes in response to thyroid hormone. Our findings show that thyroid hormone and its receptors regulate distinct events of cellular maturation across lineages, and illustrate how a single, global factor integrates seemingly divergent morphogenetic outcomes across developmental time.

developmental biology↗