Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding

Blumer, Moritz; Brown, Tom; Freitas, Mariella Bontempo; Destro, Ana Luiza Fonseca; Oliveira, Juraci Alves de; Morales, Ariadna E.; Schell, Tilman; Greve, Carola; Pippel, Martin; Jebb, David; Hecker, Nikolai; Ahmed, Alexis-Walid; Kirilenko, Bogdan; Foote, Maddy; Janke, Axel; Lim, Burton K.; Hiller, Michael

doi:10.1126/sciadv.abm6494

Cited by 39 publications

(31 citation statements)

References 141 publications

(190 reference statements)

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“…Loss of ancestral coding genes can be relevant for adaptation ( 16 – 18 ). To investigate whether gene losses may have contributed to hummingbird adaptations, we performed a genome-wide screen for genes that were specifically inactivated in the ancestral hummingbird lineage.…”

Section: Identification Of Hummingbird-specific Gene Lossesmentioning

confidence: 99%

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Osipova

Barsacchi

Brown

et al. 2023

Science

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Hummingbirds possess distinct metabolic adaptations to fuel their energy-demanding hovering flight, but the underlying genomic changes are largely unknown. Here, we generated a chromosome-level genome assembly of the long-tailed hermit and screened for genes that have been specifically inactivated in the ancestral hummingbird lineage. We discovered that FBP2 (fructose-bisphosphatase 2), which encodes a gluconeogenic muscle enzyme, was lost during a time period when hovering flight evolved. We show that FBP2 knockdown in an avian muscle cell line up-regulates glycolysis and enhances mitochondrial respiration, coincident with an increased mitochondria number. Furthermore, genes involved in mitochondrial respiration and organization have up-regulated expression in hummingbird flight muscle. Together, these results suggest that FBP2 loss was likely a key step in the evolution of metabolic muscle adaptations required for true hovering flight.

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Section: Identification Of Hummingbird-specific Gene Lossesmentioning

confidence: 99%

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Osipova

Barsacchi

Brown

et al. 2023

Science

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“…For example, as has been recently shown in agave, where a single gene encoding a phosphoenolpyruvate carboxylase enhances the plant’s climate resilience ( Liu et al, 2021 ). Not only the gain of genes, but also the loss of genes has been associated with adaptive traits, such as the evolution of particular diets in bats ( Blumer et al, 2022 ). Therefore, we consider the parallel loss of a homologous gene in two species and two geographic settings a rare find, and a step forward in understanding the genomic underpinnings of climatic tolerances in lichenized fungi.…”

Section: Discussionmentioning

confidence: 99%

Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi

et al. 2023

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IntroductionIntraspecific genomic variability affects a species’ adaptive potential toward climatic conditions. Variation in gene content across populations and environments may point at genomic adaptations to specific environments. The lichen symbiosis, a stable association of fungal and photobiont partners, offers an excellent system to study environmentally driven gene content variation. Many of these species have remarkable environmental tolerances, and often form populations across different climate zones. Here, we combine comparative and population genomics to assess the presence and absence of genes in high and low elevation genomes of two lichenized fungi of the genus Umbilicaria.MethodsThe two species have non-overlapping ranges, but occupy similar climatic niches in North America (U. phaea) and Europe (U. pustulata): high elevation populations are located in the cold temperate zone and low elevation populations in the Mediterranean zone. We assessed gene content variation along replicated elevation gradients in each of the two species, based on a total of 2050 individuals across 26 populations. Specifically, we assessed shared orthologs across species within the same climate zone, and tracked, which genes increase or decrease in abundance within populations along elevation.ResultsIn total, we found 16 orthogroups with shared orthologous genes in genomes at low elevation and 13 at high elevation. Coverage analysis revealed one ortholog that is exclusive to genomes at low elevation. Conserved domain search revealed domains common to the protein kinase superfamily. We traced the discovered ortholog in populations along five replicated elevation gradients on both continents and found that the number of this protein kinase gene linearly declined in abundance with increasing elevation, and was absent in the highest populations.DiscussionWe consider the parallel loss of an ortholog in two species and in two geographic settings a rare find, and a step forward in understanding the genomic underpinnings of climatic tolerances in lichenized fungi. In addition, the tracking of gene content variation provides a widely applicable framework for retrieving biogeographical determinants of gene presence/absence patterns. Our work provides insights into gene content variation of lichenized fungi in relation to climatic gradients, suggesting a new research direction with implications for understanding evolutionary trajectories of complex symbioses in relation to climatic change.

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“…This change in pathogen repertoire could explain the changes in the immune system genes and their regulatory mechanisms. Such pathogen load and content changes have occurred with the evolution of flight and blood-feeding in bat species (Banerjee et al, 2020;Blumer et al, 2022). Bat species have adapted to this pathogen load change by losing specific immune genes (Blumer et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Such pathogen load and content changes have occurred with the evolution of flight and blood-feeding in bat species (Banerjee et al, 2020;Blumer et al, 2022). Bat species have adapted to this pathogen load change by losing specific immune genes (Blumer et al, 2022). In the case of galliform birds, reports confirming the presence of Neisseria in the chicken are missing despite a large number of studies (Liu et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Birth and death in terminal complement pathway

Sharma

Gupta

Patil

et al. 2022

Molecular Immunology

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Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding

Cited by 39 publications

References 141 publications

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi

Birth and death in terminal complement pathway

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