More Like this

1. Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

   https://doi.org/10.1093/evlett/qrad024  

   Short, Aidan W.; Streisfeld, Matthew A. (June 2023, Evolution Letters)

   Abstract The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages. 

   more » « less
2. Captivity affects mitochondrial aerobic respiration and carotenoid metabolism in the house finch ( Haemorhous mexicanus )

   https://doi.org/10.1242/jeb.246980  

   Koch, Rebecca E.; Okegbe, Chidimma; Ramanathan, Chidambaram; Zhu, Xinyu; Hare, Ethan; Toomey, Matthew B.; Hill, Geoffrey E.; Zhang, Yufeng (April 2024, Journal of Experimental Biology)

   In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation can be 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 itself would decrease both mitochondrial performance and the abundance of red carotenoids compared to free-living birds. We found that captive-held birds 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, though we did not detect a difference in the effects of small cages versus large cages. Among captive individuals, the birds that circulated the highest concentrations of red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrate. 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. 

   more » « less
3. Mechanisms of Carotenoid Metabolism: Understanding the Links between Red Coloration, Cellular Respiration, and Individual Quality

   https://doi.org/10.1093/icb/icaf022  

   Koch, Rebecca_E; Toomey, Matthew_B; Zhang, Yufeng; Hill, Geoffrey_E (April 2025, Integrative And Comparative Biology)

   Synopsis In many species of birds, red carotenoid coloration serves as an honest signal of individual quality, but the mechanisms that link carotenoid coloration to animal performance remain poorly understood. Most birds that display red carotenoid coloration of feathers, bills, or legs ingest yellow carotenoids and metabolically convert the yellow pigments to red. Here, we review two lines of investigation that have rapidly advanced understanding of the production of red carotenoid coloration in birds, potentially providing an explanation for how red coloration serves as a signal of quality: the identification of the genes that enable birds to be red and the confirmation of links between production of red pigments and core cellular function. CYP2J19 and BDH1L were identified as key enzymes that catalyze the conversion of yellow carotenoids to red carotenoids both in the retinas of birds for enhanced color vision and in the feathers and bills of birds for ornamentation. This CYP2J19 and BDH1L pathway was shown to be the mechanism for production of red coloration in diverse species of birds and turtles. In other studies, it was shown that male House Finches (Haemorhous mexicanus) have high concentrations of red carotenoids within liver mitochondria and that redness is positively associated with mitochondrial function. These observations suggested that the CYP2J19 and BDH1L pathway might be tightly associated with mitochondrial function. However, it was subsequently discovered that male House Finches do not use the CYP2J19 and BDH1L pathway to produce red pigments and that both CYP2J19 and BDH1L localize in the endoplasmic reticulum, not the mitochondria. Thus, we have the most detailed understanding of links between cellular function and redness in a bird species for which the enzymes to convert yellow to red pigments remain unknown, while we have the best understanding of the enzymatic pathways to red in species for which links to cellular function are largely unstudied. Deducing whether and how signals of quality arise from these distinct mechanisms of ornamental coloration is a current challenge for scientists interested in the evolution of honest signaling. 

   more » « less
4. Eavesdropping on Referential Yellow Warbler Alarm Calls by Red-Winged Blackbirds Is Mediated by Brood Parasitism Risk

   https://doi.org/10.3389/fevo.2021.706170  

   Lawson, Shelby L.; Enos, Janice K.; Gill, Sharon A.; Hauber, Mark E. (October 2021, Frontiers in Ecology and Evolution)

   Referential alarm calls that denote specific types of dangers are common across diverse vertebrate lineages. Different alarm calls can indicate a variety of threats, which often require specific actions to evade. Thus, to benefit from the call, listeners of referential alarm calls must be able to decode the signaled threat and respond to it in an appropriate manner. Yellow warblers ( Setophaga petechia ) produce referential “seet” calls that signal to conspecifics the presence of nearby obligate brood parasitic brown-headed cowbirds ( Molothrus ater ), which lay their eggs in the nests of other species, including yellow warblers. Our previous playback experiments have found that red-winged blackbirds ( Agelaius phoeniceus ), a species also parasitized by brown-headed cowbirds, eavesdrop upon and respond strongly to yellow warbler seet calls during the incubation stage of breeding with aggression similar to responses to both cowbird chatters and predator calls. To assess whether red-winged blackbird responses to seet calls vary with their own risk of brood parasitism, we presented the same playbacks during the nestling stage of breeding (when the risk of brood parasitism is lower than during incubation). As predicted, we found that blackbirds mediated their aggression toward both cowbird chatter calls and the warblers’ anti-parasitic referential alarm calls in parallel with the low current risk of brood parasitism during the nestling stage. These results further support that red-winged blackbirds flexibly respond to yellow warbler antiparasitic referential calls as a frontline defense against brood parasitism at their own nests. 

   more » « less
5. Testosterone Coordinates Gene Expression Across Different Tissues to Produce Carotenoid-Based Red Ornamentation

   https://doi.org/10.1093/molbev/msad056  

   Khalil, Sarah; Enbody, Erik D; Frankl-Vilches, Carolina; Welklin, Joseph F; Koch, Rebecca E; Toomey, Matthew B; Sin, Simon Yung; Edwards, Scott V; Gahr, Manfred; Schwabl, Hubert; et al (April 2023, Molecular Biology and Evolution)

   Parsch, John (Ed.)

   Abstract Carotenoid pigments underlie most of the red, orange, and yellow visual signals used in mate choice in vertebrates. However, many of the underlying processes surrounding the production of carotenoid-based traits remain unclear due to the complex nature of carotenoid uptake, metabolism, and deposition across tissues. Here, we leverage the ability to experimentally induce the production of a carotenoid-based red plumage patch in the red-backed fairywren (Malurus melanocephalus), a songbird in which red plumage is an important male sexual signal. We experimentally elevated testosterone in unornamented males lacking red plumage to induce the production of ornamentation and compared gene expression in both the liver and feather follicles between unornamented control males, testosterone-implanted males, and naturally ornamented males. We show that testosterone upregulates the expression of CYP2J19, a gene known to be involved in ketocarotenoid metabolism, and a putative carotenoid processing gene (ELOVL6) in the liver, and also regulates the expression of putative carotenoid transporter genes in red feather follicles on the back, including ABCG1. In black feathers, carotenoid-related genes are downregulated and melanin genes upregulated, but we find that carotenoids are still present in the feathers. This may be due to the activity of the carotenoid-cleaving enzyme BCO2 in black feathers. Our study provides a first working model of a pathway for carotenoid-based trait production in free-living birds, implicates testosterone as a key regulator of carotenoid-associated gene expression, and suggests hormones may coordinate the many processes that underlie the production of these traits across multiple tissues. 

   more » « less