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Genomic signatures of the evolution of a diurnal lifestyle in Strigiformes.

ABSTRACT: Understanding the targets of selection associated with changes in behavioral traits represents an important challenge of current evolutionary research. Owls (Strigiformes) are a diverse group of birds, most of which are considered nocturnal raptors. However, a few owl species independently adopted a diurnal lifestyle in their recent evolutionary history. We searched for signals of accelerated rates of evolution associated with a diurnal lifestyle using a genome-wide comparative approach. We estimated substitution rates in coding and noncoding conserved regions of the genome of seven owl species, including three diurnal species. Substitution rates of the noncoding elements were more accelerated than those of protein-coding genes. We identified new, owl-specific conserved noncoding elements as candidates of parallel evolution during the emergence of diurnality in owls. Our results shed light on the molecular basis of adaptation to a new niche and highlight the importance of regulatory elements for evolutionary changes in behavior. These elements were often involved in the neuronal development of the brain.

SUBMITTER: Espindola-Hernandez P

PROVIDER: S-EPMC9339318 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Genomic signatures of the evolution of a diurnal lifestyle in Strigiformes.

Espíndola-Hernández Pamela P Mueller Jakob C JC Kempenaers Bart B

G3 (Bethesda, Md.) 20220701 8

Understanding the targets of selection associated with changes in behavioral traits represents an important challenge of current evolutionary research. Owls (Strigiformes) are a diverse group of birds, most of which are considered nocturnal raptors. However, a few owl species independently adopted a diurnal lifestyle in their recent evolutionary history. We searched for signals of accelerated rates of evolution associated with a diurnal lifestyle using a genome-wide comparative approach. We esti ...[more]

PMID: 35640557

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Project description:BackgroundPangolin is one of the most endangered mammals with many peculiar characteristics, yet the understanding of its sensory systems is still superficial. Studying the genomic basis of adaptation and evolution of pangolin's sensory system is expected to provide further potential assistance for their conservation in the future.ResultsIn this study, we performed a comprehensive comparative genomic analysis to explore the signature of sensory adaptation and evolution in pangolins. By comparing with the aardvark, Cape golden mole, and short-beaked echidna, 124 and 152 expanded gene families were detected in the genome of the Chinese and Malayan pangolins, respectively. The enrichment analyses showed olfactory-related genomic convergence among five concerned mammals. We found 769 and 733 intact OR genes, and 704 and 475 OR pseudogenes in the Chinese and Malayan pangolin species, respectively. Compared to other mammals, far more intact members of OR6 and OR14 were identified in pangolins, particularly for four genes with large copy numbers (OR6C2, OR14A2, OR14C36, and OR14L1). On the genome-wide scale, 1,523, 1,887, 1,110, and 2,732 genes were detected under positive selection (PSGs), intensified selection (ISGs), rapid evolution (REGs), and relaxed selection (RSGs) in pangolins. GO terms associated with visual perception were enriched in PSGs, ISGs, and REGs. Those related to rhythm and sound perception were enriched in both ISGs and REGs, ear development and morphogenesis were enriched in ISGs, and mechanical stimulus and temperature adaptation were enriched in RSGs. The convergence of two vision-related PSGs (OPN4 and ATXN7), with more than one parallel substituted site, was detected among five concerned mammals. Additionally, the absence of intact genes of PKD1L3, PKD2L1, and TAS1R2 and just six single-copy TAS2Rs (TAS2R1, TAS2R4, TAS2R7, TAS2R38, TAS2R40, and TAS2R46) were found in pangolins. Interestingly, we found two large insertions in TAS1R3, distributed in the N-terminal ectodomain, just in pangolins.ConclusionsWe found new features related to the adaptation and evolution of pangolin-specific sensory characteristics across the genome. These are expected to provide valuable and useful genome-wide genetic information for the future breeding and conservation of pangolins.

Project description:Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands," many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.

Dataset Information

Genomic signatures of the evolution of a diurnal lifestyle in Strigiformes.

Publications

Genomic signatures of the evolution of a diurnal lifestyle in Strigiformes.

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