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Gene duplication is an important process of molecular evolutionary change, though identifying these events and their functional implications remains challenging. Studies on gene duplication more often focus on the presence of paralogous genes within the genomes and less frequently explore shifts in expression. We investigated the evolutionary history of calsequestrin (CASQ), a crucial calcium-binding protein in the junctional sarcoplasmic reticulum of muscle tissues. CASQ exists in jawed vertebrates as subfunctionalized paralogs CASQ1 and CASQ2 expressed primarily in skeletal and cardiac muscles, respectively. We used an enhanced sequence dataset to support initial duplication of CASQl in a jawed fish ancestor prior to the divergence of cartilaginous fishes. Surprisingly, we find CASQ2 is the predominant skeletal muscle paralog in birds, while CASQ1 is either absent or effectively nonfunctional. Changes in the amino acid composition and electronegativity of avian CASQ2 suggest enhancement to calcium-binding properties that preceded the loss of CASQ1. We identify this phenomenon as CASQ2 “synfunctionalization,” where one paralog functionally replaces another. While additional studies are needed to fully understand the dynamics of CASQ1 and CASQ2 in bird muscles, the long and consistent history of CASQ subfunctions outside of birds indicate a substantial evolutionary pressure on calcium-cycling processes in muscle tissues, likely connected to increased avian cardiovascular and metabolic demands. Our study provides an important insight into the molecular evolution of birds and shows how gene expression patterns can be comparatively studied across phylum-scale deep time to reveal key evolutionary events 

Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Flowering plant reproduction depends on the ability of pollen grains to generate a pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. We used tomato as amodel fruit croptodeterminehowhigh temperature affects the pollen tube growthphase, takingadvantage of cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to high temperature solely during the pollen tube growth phase limits fruit biomass and seed set more significantly in thermosensitive cultivars than in thermotolerant cultivars. Importantly, we found that pollen tubes from the thermotolerantTamaulipas cultivar have enhanced growth in vivo and in vitro under high temperature. Analysis of the pollen tube transcriptome’s response to high temperature allowed us to define two responsemodes (enhanced induction of stress responses and higher basal levels of growth pathways repressed by heat stress) associated with reproductive thermotolerance. Importantly, we define key components of the pollen tube stress response, identifyingenhancedreactive oxygenspecies (ROS)homeostasis andpollen tubecallose synthesis and deposition as important components of reproductive thermotolerance in Tamaulipas. Our work identifies the pollen tube growth phase as a viable target to enhance reproductive thermotolerance and delineates key pathways that are altered in crop varieties capable of fruiting under high-temperature conditions. 

In a hybrid zone between two tropical lekking birds, yellow male plumage of one species has introgressed asymmetrically replacing white plumage of another via sexual selection. Here, we present a detailed analysis of the plumage trait to uncover its physical and genetic bases and trace its evolutionary history. We determine that the carotenoid lutein underlies the yellow phenotype and describe microstructural feather features likely to enhance color appearance. These same features reduce predicted water shedding capacity of feathers, a potential liability in the tropics. Through genome-scale DNA sequencing of hybrids and each species in the genus, we identifyBCO2as the major gene responsible for the color polymorphism. TheBCO2gene tree and genome-wide allele frequency patterns suggest that carotenoid-pigmented collars initially arose in a third species and reached the hybrid zone through historical gene flow. Complex interplay between sexual selection and hybridization has thus shaped phenotypes of these species, where conspicuous sexual traits are key to male reproductive success. 

Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The tomato (Solanum lycopersicum) anthocyanin reduced (are) mutant harbors a mutation in FLAVANONE 3-HYDROXYLASE (F3H), resulting in impaired flavonol antioxidant biosynthesis. The are mutant has reduced pollen performance and seed set relative to the VF36 parental line, phenotypes that are accentuated at elevated temperatures. Transformation of are with the wild-type F3H gene, or chemical complementation with flavonols, prevented temperature-dependent reactive oxygen species (ROS) accumulation in pollen and restored the reduced viability, germination, and tube elongation of are to VF36 levels. Overexpression of F3H in VF36 prevented temperature-driven ROS increases and impaired pollen performance, revealing that flavonol biosynthesis promotes thermotolerance. Although stigmas of are had reduced flavonol and elevated ROS levels, the growth of are pollen tubes was similarly impaired in both are and VF36 pistils. RNA-seq was performed at optimal and stress temperatures in are, VF36, and the F3H overexpression line at multiple timepoints across pollen tube elongation. The number of differentially expressed genes increased over time under elevated temperatures in all genotypes, with the greatest number in are. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that lead to reproductive failure. 

Identifying the molecular process of complex trait evolution is a core goal of biology. However, pinpointing the specific context and timing of trait-associated changes within the molecular evolutionary history of an organism remains an elusive goal. We study this topic by exploring the molecular basis of elaborate courtship evolution, which represents an extraordinary example of trait innovation. Within the behaviorally diverse radiation of Central and South American manakin birds, species from two separate lineages beat their wings together using specialized “superfast” muscles to generate a “snap” that helps attract mates. Here, we develop an empirical approach to analyze phylogenetic lineage-specific shifts in gene expression in the key snap-performing muscle and then integrate these findings with comparative transcriptomic sequence analysis. We find that rapid wing displays are associated with changes to a wide range of molecular processes that underlie extreme muscle performance, including changes to calcium trafficking, myocyte homeostasis and metabolism, and hormone action. We furthermore show that these changes occur gradually in a layered manner across the species history, wherein which ancestral genetic changes to many of these molecular systems are built upon by later species-specific shifts that likely finalized the process of display performance adaptation. Our study demonstrates the potential for combining phylogenetic modeling of tissue-specific gene expression shifts with phylogenetic analysis of lineage-specific sequence changes to reveal holistic evolutionary histories of complex traits.