Biology subjects

Hill, G. E.

Publications and source records attributed to Hill, G. E..

6 recordsLinked to original sources

bioRxiv2024

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↗

bioRxiv2024

Diversifying selection and adaptive introgression of carotenoid-processing genes underlie the evolution of bill color in the long-tailed finch

Carotenoid pigmentation produces the yellow and red coloration of birds and other vertebrates, but our understanding of the genetic architecture of carotenoid ornamentation is largely limited to studies of novel color variants observed in captively bred populations. The complexity of carotenoid-based color evolution in nature remains poorly characterized. Here, we examine the long-tailed finch Poephila acuticauda, an Australian songbird with two hybridizing subspecies that differ in bill coloration: yellow in western subspecies acuticauda and red in eastern subspecies hecki. We characterize the carotenoid composition of each subspecies and find that yellow bills can be explained by the loss of C(4)-oxidation, thus blocking yellow dietary pigments from being metabolized to red. Combining linked-read genomic sequencing and reflectance spectrophotometry measurements of bill color collected from wild-sampled finches and laboratory crosses, we identify four loci that together explain 53% of variance in this trait. The two loci of largest effect contain the genes CYP2J19, an essential enzyme for the ketolation via C(4)-oxidation of dietary carotenoids, and TTC39B, an enhancer of ketocarotenoid production. Evolutionary genealogy reconstruction indicates that the red-billed phenotype is ancestral and yellow alleles at both CYP2J19 and TTC39B arose and fixed in acuticauda approximately 100 kya. Yellow alleles then introgressed into hecki less than 5 kya. Across all four loci, acuticauda derived variants show evidence of selective sweeps, implying that yellow bill coloration has been favored by natural selection. Our study suggests that the frequent adaptive evolutionary transitions between red and yellow ornamentation in nature can have a simple genetic basis. SignificanceWe studied variation in carotenoid ornamentation of an Australian songbird with two hybridizing subspecies that differ in bill color: one yellow and the other red. We identified a single metabolic process, C(4)-oxidation, underlying the distinct carotenoid composition of these two bill colors. Genetic association mapping revealed four major effect loci that explained most of the observed variation the trait, including the oxidative ketolation enzyme CYP2J19 and the carotenoid ketolation enhancer gene TTC39B. Evolutionary reconstruction indicates that yellow alleles are derived, ancient (~100 kya), and under positive selection. This has driven their recent (<5 kya) adaptive introgression across the hybrid zone. These findings have important implications for understanding the role of natural selection in phenotypic evolution in natural systems.

evolutionary biology↗

bioRxiv2023

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↗

bioRxiv2023

Evolution of the CRISPR-Cas9 defence system following a bacterial host shift

CRISPR-Cas systems are bacterial defences that target bacteriophages and mobile genetic elements. How these defences evolve in novel host environments remains, however, unknown. We studied the evolution of the CRISPR-Cas system in Mycoplasma gallisepticum, a bacterial pathogen of poultry that jumped into a passerine host [~]30 years ago. Over the decade following the host shift, all isolates displayed a functional CRISPR-Cas system were found not only to harbour completely new sets of spacers, but the DNA protospacer adjacent motif (PAM) recognised by the main effector MgCas9 was also different. These changes in CRISPR-Cas diversity and specificity are consistent with a change in the community of phages and mobile elements infecting M. gallisepticum as it colonised the novel host. In the years following the host shift, we also detected a gradual rise in isolates displaying non-functional MgCas9. After 12 years, all circulating isolates harboured inactive forms only. This loss of CRISPR-Cas function comes at a time when the passerine host is known to have evolved widespread resistance, which in turn drove the evolution of increasing M. gallisepticum virulence through antagonistic coevolution. Such striking concordance in the rise of inactivated forms of CRISPR-Cas and the evolution of host resistance suggests that inactivation of the CRISPR-Cas system was necessary for enabling adaptive bacterial responses to host-driven selection. We highlight the need to consider both host and pathogen selection pressures on bacteria for understanding the evolution of CRISPR-Cas systems and the key factors driving the emergence of a pathogenic bacterium in a novel host. Data summaryThe authors confirm all supporting data and protocols have been provided within the article or through supplementary data files available in the online version of this article. GenBank accession numbers of all publicly available M. gallisepticum genomes are listed in Table S3. Sequences of the CRISPR locus of other strains are also provided in Table S3. Impact statementMycoplasma are minimal bacteria involved in many diseases affecting humans and a wide diversity of animals. In this paper, we report the evolution of the Type II CRISPR-Cas system of the bird pathogen, Mycoplasma gallisepticum, following an host jump from its original poultry host into its novel house finch host in the early 90s. Instances in which bacterial pathogens have been documented to jump into and subsequently adapt to a new host are rare, and the well documented case of M. gallisepticum is a unique model to evaluate the effect of any dramatic host environmental change on bacterial CRISPR-Cas defence systems. First, we performed in silico analyses on an extended set of 98 M. gallisepticum genomes to better understand the evolution of the CRISPR-Cas9 system in the novel finch host. We documented several evolutionary events leading to the drastic divergence of spacer sets present in poultry and house finch arrays, as well as the progressive inactivation of the CRISPR-Cas system after 12 years in the novel finch host. Second, using in vitro and in vivo assays, we demonstrated that the evolution of the MgCas9 PI domain, involved in the protospacer adjacent motif (PAM) recognition has led to a major change in the defence system, with a modification of the recognized PAM in the novel host. Such radical change in the CRISPR-Cas defence system of M. gallisepticum may have implications for the its rapid adaptation to its novel host. Together, our results highlight the need to consider not only the host-driven selection pressures a bacterium experiences, but also the complex interplay between phages and defence systems for better understanding the key factors driving the emergence of a pathogenic bacterium in a novel host.

microbiology↗

bioRxiv2019

Plumage redness signals mitochondrial function in the House Finch

Carotenoid coloration is widely recognized as a signal of individual condition in various animals, but despite decades of study, the mechanisms that link carotenoid coloration to condition remain unresolved. Most birds with red feathers convert yellow dietary carotenoids to red carotenoids in an oxidation process requiring the gene encoding the putative cytochrome P450 enzyme CYP2J19. Here, we tested the hypothesis that the process of carotenoid oxidation and feather pigmentation is functionally linked to mitochondrial performance. Consistent with this hypothesis, we observed high levels of red ketolated carotenoids associated with the hepatic mitochondria of molting wild house finches (Haemorhous mexicanus), and upon fractionation, we found the highest concentration of ketolated carotenoids in the inner mitochondrial membrane. We further found that the redness of growing feathers was positively related to the performance of liver mitochondria. Structural modeling of CYP2J19 supports a direct role of this protein in carotenoid ketolation that may be functionally linked to cellular respiration. These observations suggest that feather coloration serves as a signal of core functionality through inexorable links to cellular respiration in the mitochondria.

evolutionary biology↗

bioRxiv2017

On the bioconversion of dietary carotenoids to astaxanthin and its distribution in the marine copepod, Tigriopus californicus

Red carotenoid-based coloration is widely distributed across marine and terrestrial animals and has taken a prominent role in studies of how phenotypic traits evolve in response to natural and sexual selection. Key to these studies is an understanding of the physiological mechanisms that give rise to red coloration, yet an ideal model system for such work has not been identified. The red marine copepod Tigriopus californicus is used as a model system for studies in ecotoxicology, genetics, and physiology, but the mechanisms involved in its bright red coloration have not been well studied. Like nearly all animals that display red carotenoid coloration, T. californicus likely convert yellow carotenoids present in their algal diet to red carotenoids. We conducted precursor/product feeding experiments to demonstrate that T. californicus bioconverts dietary carotenoids to the red carotenoid, astaxanthin. In separate treatment groups, copepods were fed carotenoids that are precursors to specific astaxanthin bioconversion pathways. We found that copepods from each precursor pigment group produced astaxanthin, and that the amount produced depended on which carotenoid was supplemented. We also describe the distribution of astaxanthin in developing egg sacs and show that the red color of the naupliar eyespot is not due to astaxanthin. We briefly discuss the potential of Tigriopus californicus to serve as a model system for the study of carotenoid metabolism in animals.

zoology↗